Topic Highlight Open Access
Copyright ©2014 Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Pathophysiol. Aug 15, 2014; 5(3): 200-204
Published online Aug 15, 2014. doi: 10.4291/wjgp.v5.i3.200
Laparoscopic surgery in the management of Crohn's disease
James Y Lim, Joseph Kim, Scott Q Nguyen, Department of Surgery, Icahn School of Medicine at Mount Sinai, New York, NY 10029, United States
Author contributions: Lim JY performed the searches and prepared the initial draft; Kim J and Nguyen SQ edited and supplemented the manuscript.
Correspondence to: Scott Q Nguyen, MD, Department of Surgery, Icahn School of Medicine at Mount Sinai, 1 Gustave Levy Place, New York, NY 10029, United States. scott.nguyen@mountsinai.org
Telephone: +1-212-2418672 Fax: +1-212-2415979
Received: December 29, 2013
Revised: April 9, 2014
Accepted: May 29, 2014
Published online: August 15, 2014
Processing time: 249 Days and 3.9 Hours

Abstract

Crohn’s disease is a chronic inflammatory bowel disease with surgery still frequently necessary in its treatment. Since the 1990’s, laparoscopic surgery has become increasingly common for primary resections in patients with Crohn’s disease and has now become the standard of care. Studies have shown no difference in recurrence rates when compared to open surgery and benefits include shorter hospital stay, lower rates of wound infection and decreased time to bowel function. This review highlights studies comparing the laparoscopic approach to the open approach in specific situations, including cases of complicated Crohn’s disease.

Key Words: Crohn’s; Laparoscopy; Surgery; Colon; Ileum

Core tip: Laparoscopy is now increasingly used in cases of Crohn’s disease. Recurrence rates are similar to that of open surgery and studies have shown benefits of decreased hospital stay as well as earlier bowel function. This review highlights several studies that looked at patients who underwent ileocolic and colon resections as well as more complicated cases of Crohn’s.



INTRODUCTION

Crohn’s disease is an autoimmune disorder that causes chronic transmural inflammation of the gastrointestinal tract and makes up one of the two main components of inflammatory bowel disease[1]. The terminal ileum and proximal colon are the most frequently affected and initial diagnosis is made early, between the ages of 20-30[2]. Despite the advances in medical therapies with increasingly new immunomodulator use, the rate of refractory disease requiring surgery has not changed over the years[3]. Surgery is still common and up to 80% of patients with Crohn’s disease will require an operation during their lifetime, with 15%-20% requiring an operation within the first year after diagnosis[4-6]. Of those patients that undergo surgery, studies have shown that approximately 40%-50% will likely need additional surgical intervention within 10-15 years[7,8]. The likelihood of a second surgery within one’s lifetime is high, with several studies having identified the median age of first surgical resection to be in a patient’s third decade[6,9].

Initially, laparoscopic surgery was not attempted for Crohn’s disease due to the intraoperative characteristics that made a laparoscopic approach challenging. These findings often included extensive inflammation, enteric fistulae, thickened mesentery, and skip lesions throughout the bowel[10]. This belief has changed over time and laparoscopy has become increasingly accepted in patients with Crohn’s disease as the use of laparoscopy in a majority of gastrointestinal procedures has become standard[11]. Crohn’s patients are typically young and benefit from a laparoscopic procedure that reduces scar and adhesion formation. In addition, given their high risk of surgical recurrence, Crohn’s patients benefit from surgical approaches that maximize abdominal wall integrity[2,10,12,13].

This article review will evaluate surgical resections as well as common surgical scenarios commonly seen with Crohn’s disease and compare the laparoscopic and open approaches. A search was conducted in the PubMed, Cochrane, MEDLINE, and Scopus libraries with the following individual and combined key words: Crohn’s disease, laparoscopy, surgery, cost, colon, ileocolic, fistula, recurrent, small bowel, outcome, minimally invasive surgery, inflammatory bowel disease, randomized, metaanalysis. References cited in the articles retrieved were also searched in order to identify other potential sources of information. The results were limited to human studies available in English.

LAPAROSCOPIC ILEOCOLIC RESECTIONS

One of the first randomized trials comparing laparoscopic resections to open resections for refractory ileocolic disease was published in 2001 by Milsom et al[14] Sixty patients were randomized to undergo either laparoscopic or open procedures. The authors reported improved morbidity rates and hospital length of stay rates in the laparoscopic group, although the anastomotic leak rate was similar between the two groups. Length of surgery favored the open group. Long term follow up showed no difference between the groups in terms of disease recurrence rates.

A similar long term prospective study undertaken from 1999-2003 in the Netherlands showed similar results of no difference in overall disease recurrence between the laparoscopic and the open groups. Additionally, there were fewer incidences of small bowel obstruction and incisional hernias in the laparoscopic group. Overall, patient quality of life and cosmesis scores favored the laparoscopic group[15].

One of the weaknesses of these randomized prospective studies is that the overall number of patients treated was small. However, metaanalysis studies with a larger number of subjects show that these findings for laparoscopic surgeries are consistent. In a large metaanalysis by Tilney, data from over 15 different studies looking specifically at laparoscopic ileocolic resections was compiled. The analysis included 783 patients, 338 (43.2%) of which had undergone laparoscopic resection. The overall conversion rate to open surgery was 6.8%. As seen in earlier studies, overall surgery duration was longer in the laparoscopic group with a difference of 29.6 min. Perioperative complications and anastomotic leak rates were similar between the two groups. Benefits of laparoscopy were significantly shorter time till bowel function was regained and a shorter hospital stay by 2.7 d[16].

These findings are also supported by other smaller prospective and retrospective studies comparing open vs laparoscopic ileocolic resections in patients with Crohn’s disease. There were no differences in morbidity and mortality. Furthermore lengths of time till return of bowel function and hospital stay were consistently shorter in the laparoscopic groups[17-20].

More recently, data reviewed from the National Surgical Quality Improvement Program from 2005-2009 compiled perioperative results from over 1900 ileocolic resections for Crohn’s disease, 34% of which were performed laparoscopically. On multivariate analysis, the laparoscopic group was associated with an overall decrease in major and minor perioperative complications as well as a significant decrease in overall hospital stay by 1.08 d[21].

Long term studies following open and laparoscopic ileocolic resection patients showed no difference in recurrence rates[22,23]. In one study, the average time to recurrence was 60 mo in the laparoscopic group and 62 mo in the open group. Another study reported the average five year recurrence rates to be 29.1% in laparoscopic patients and 27.7% in open patients. Median times to recurrence were 48 and 56 mo, respectively. These times were not significant with a P-value of 0.9104. Of note, the laparoscopic group was found to have lower bowel obstruction rates over that time period[18].

LAPAROSCOPIC COLON RESECTIONS

Much of the literature focuses on laparoscopic surgery at the ileocolic region. Because Crohn’s disease can affect any part of the gastrointestinal tract, other anatomical locations can pose different challenges. Acute colitis rates in Crohn’s disease patients ranges from 5% to 10%[24]. Given the larger size of the colon and potentially broader thicker diseased mesentery of the colon, laparoscopic surgery for Crohn’s colitis was slower to become accepted.

One of the earliest studies comparing minimally invasive surgery in Crohn’s colitis to open surgery was in 2007. This study case matched 27 patients based on various patient factors including comorbidities and types of surgery, looking at patients only with disease in the colon. The authors found that although overall surgery was longer in the laparoscopic group, complications and estimated blood loss were the same in both groups. Length of hospital stay was significantly shorter in the laparoscopic group when 30 d readmissions were included[25].

Another study retrospectively looked at 92 patients with Crohn’s disease that underwent minimally invasive colon resections. Forty-three cases (47%) were total colectomies, 17 (18%) were subtotal colectomies, 32 (35%) were segmental resections. There were 15 conversions to open resections, but conversions were not associated with longer hospital stay or increased postoperative complications. Five patients required reoperation, three for obstruction and two for anastomotic leak. The only prognostic factor for a complicated hospital course was evidence of perianal disease and 30-d mortality was zero[26].

One of the largest studies looking at laparoscopic colon resections in patients with Crohn’s disease prospectively compared 55 laparoscopic resections to 70 open resections. The conversion rate to open resection of 10.9 was similar to that for ileocolic resections. Of note, 34.5% of patients who underwent laparoscopic surgery had had prior abdominal surgery as compared to 65.7% of the open group. This is one of the weaknesses of this study as surgeon preference dictated which procedure was performed. Although there was likely selection bias, the laparoscopic group was associated with similar benefits that were identified in the randomized studies for ileocolic resections. These benefits included less intraoperative blood loss, shorter hospital stays and quicker return of bowel function after surgery in the laparoscopic group[27].

LAPAROSCOPIC SURGERY FOR FISTULIZING DISEASE

Enteric fistulas are challenging complications in Crohn’s patients as this finding often implies the presence of a large inflammatory mass, a history of prior surgeries, or use of steroids-all of which can make the surgery technically difficult. Surgery for enteric fistulas requires resection of the involved segment and primary anastomosis in the elective setting. Fistulas involving other organs are treated with bowel resection of the involved segment and primary repair of the other involved organ[10,28]. Some studies have cited intraoperative discovery of an intraabdominal abscess or fistula as an independent risk factor for conversion from a laparoscopic procedure[29]. In addition, a recent consensus conference was unable to recommend a laparoscopic approach for cases of complex Crohn’s disease[30].

A laparoscopic approach in these patients with complicated Crohn’s can be treacherous but as surgeons have become more skilled with laparoscopy, more studies have shown its feasibility. One retrospective review looked at 72 patients who underwent laparoscopic surgery for enteric fistulas. This study included enterocolic, ileo-ileal, enterocutaneous, ileovesical, colovesical, colocutaneous, and colovaginal fistulas. Prior abdominal surgery was present in 39.7% of the patients. Approximately 30% of the patients had multiple fistulas and 12.3% of those underwent multiple resections. The rate of conversion to open resection was low at 4.1% and overall morbidity was 11%[28].

In a more recent case-matched study 11 patients presenting with 13 fistulas were matched to 22 controls with non-fistulizing disease according to age, sex, nutritional state, steroid use, and type of laparoscopic resection[31]. Although the sample size was small, the authors were unable to show any difference in operative time, conversion rates, or morbidity rates between the two groups.

A larger prospective comparative study compared laparoscopic ileocolonic resections in patients with complex Crohn’s disease (abscess and/or fistula) to patients without complex Crohn’s disease. There was no significant difference in postoperative complications but overall operative time, conversion rates, and frequency of temporary stoma creation were all significantly increased in the complex Crohn’s group[32]. These findings are suggestive of a more challenging operation, although the lack of increased morbidity demonstrates that a laparoscopic approach is still feasible. This is an area that needs to be continued to be studied.

LAPAROSCOPIC SURGERY FOR RECURRENT DISEASE

As indications for laparoscopic surgery in patients with Crohn’s disease expands, its use in patients with recurrent disease seems natural. Several studies have compared laparoscopic resection to open resection for recurrent disease with no significant difference in surgical outcomes[33,34]. The reported conversion rates within these studies ranged from 6.7%-42% with the most common reasons for conversion being adhesions, intraoperative discovery of fistula/abscess, or need for associated bowel resection. In general, the conversion rate for recurrent Crohn’s disease was similar to numbers seen in surgeries for initial disease. Only in one study was the conversion rate higher in the recurrent disease group and risk factors for conversion were age greater than 40, repeat resection for recurrent disease, and operative findings of an abscess[35].

Laparoscopic surgery is also possible in patients whose primary operation was a midline laparotomy. A recent study compared laparoscopic vs open surgery for patients with recurrent Crohn’s disease where their primary surgery was a bowel resection through a midline laparotomy. The study was a retrospective case matched study comparing 26 patients who underwent laparoscopic resection to 26 patients that underwent open resection. Both groups had comparable demographics in terms of comorbidities and prior number of abdominal surgeries. Of note, the recovery benefits of shorter hospital stay and earlier return of bowel function that are seen in all other studies were not maintained in the laparoscopic group. However, there was a significant decrease in wound complication rates when compared to the open group[36].

ROLE OF SINGLE INCISION SURGERY IN CROHN’S DISEASE

As the role of laparoscopy has increased in patients with Crohn’s disease, other advances such as single incision surgeries have also been studied in these patients. Of the few studies published, there is a significant amount of heterogeneity in terms of the technical aspects of the procedures and long term data is not available. Initial results though, show that the single incision approach is feasible without a large increase in complications and with the benefit of decreased postoperative analgesia. Other studies have shown that complication profile is similar to laparoscopic surgery with the only advantage appearing to be the decreased number of trocar sites while all other factors were equivalent[8,37-39].

COST EFFECTIVENESS OF LAPAROSCOPIC SURGERY IN CROHN’S DISEASE

The overall cost of care for Crohn’s disease continues to increase, with some estimates placing the annual cost in the United States anywhere from $10-15.9 billion and $2.1-16.7 billion in Europe[40-42]. These estimates are expected to increase as newer biologic drugs are increasingly available and used in management[43]. Of these costs, hospitalizations accounted for 53%-66% of the total in the United States with an average of $37459 per hospitalization[41].

Laparoscopy has the potential to decrease these costs per hospitalization as studies have shown that, when compared to open surgeries, laparoscopic surgeries reduce length of hospital stays and concomitant complications. A recent study comparing laparoscopic to open cases found the difference in hospital charges were significantly different, on average $27575 vs $38713 respectively[44]. These savings are consistent with those seen in colorectal cancer resections when comparing laparoscopic to open surgeries[45]. These savings can be potentially further reduced with the increasing adoption of single port surgery as well[46].

CONCLUSION

Current literature lacks a large number of randomized trials, but the consistent outcomes seen in the numerous retrospective studies and the small number of randomized studies shows that minimally invasive surgical approaches for Crohn’s disease patients are both feasible and safe. It is important to remember that patient selection and surgeon experience are important factors for successful laparoscopic surgery. Complicated Crohn’s cases with recurrent disease and enteric fistulas require knowledge of advanced laparoscopic techniques. The primary benefits of laparoscopic surgery over open surgery are quicker return to bowel function, decreased wound infection rates and shorter hospital stays. With no difference in recurrence rates seen, laparoscopy is emerging as the standard approach for patients with Crohn’s disease for initial surgery, and even in select cases of patients with recurrent and complicated Crohn’s disease.

Footnotes

P- Reviewer: Agresta F, Amornyotin S, Filik L, Sajid MS S- Editor: Ji FF L- Editor: A E- Editor: Lu YJ

References
1.  Bandzar S, Gupta S, Platt MO. Crohn’s disease: a review of treatment options and current research. Cell Immunol. 2013;286:45-52.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 46]  [Cited by in F6Publishing: 46]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
2.  Spinelli A, Sacchi M, Bazzi P, Leone N, Danese S, Montorsi M. Laparoscopic surgery for recurrent Crohn’s disease. Gastroenterol Res Pract. 2012;2012:381017.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 14]  [Article Influence: 1.2]  [Reference Citation Analysis (0)]
3.  Rink AD, Fischer IR, Vestweber B, Vestweber KH. Long-term outcome of laparoscopic ileocecal resection for Crohn’s disease before the era of biologics. Int J Colorectal Dis. 2014;29:127-132.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 11]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
4.  Tavernier M, Lebreton G, Alves A. Laparoscopic surgery for complex Crohn’s disease. J Visc Surg. 2013;150:389-393.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18]  [Cited by in F6Publishing: 22]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
5.  Sica GS, Biancone L. Surgery for inflammatory bowel disease in the era of laparoscopy. World J Gastroenterol. 2013;19:2445-2448.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 58]  [Cited by in F6Publishing: 54]  [Article Influence: 4.9]  [Reference Citation Analysis (1)]
6.  Patel SV, Patel SV, Ramagopalan SV, Ott MC. Laparoscopic surgery for Crohn’s disease: a meta-analysis of perioperative complications and long term outcomes compared with open surgery. BMC Surg. 2013;13:14.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 67]  [Cited by in F6Publishing: 73]  [Article Influence: 6.6]  [Reference Citation Analysis (0)]
7.  Hasegawa H, Watanabe M, Nishibori H, Okabayashi K, Hibi T, Kitajima M. Laparoscopic surgery for recurrent Crohn’s disease. Br J Surg. 2003;90:970-973.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 60]  [Cited by in F6Publishing: 68]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
8.  Neumann PA, Rijcken EJ, Bruewer M. Current status of laparoscopic surgery for patients with Crohn’s disease. Int J Colorectal Dis. 2013;28:599-610.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 14]  [Cited by in F6Publishing: 14]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
9.  Bernell O, Lapidus A, Hellers G. Risk factors for surgery and recurrence in 907 patients with primary ileocaecal Crohn’s disease. Br J Surg. 2000;87:1697-1701.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 241]  [Cited by in F6Publishing: 234]  [Article Influence: 9.8]  [Reference Citation Analysis (0)]
10.  Nguyen SQ, Teitelbaum E, Sabnis AA, Bonaccorso A, Tabrizian P, Salky B. Laparoscopic resection for Crohn’s disease: an experience with 335 cases. Surg Endosc. 2009;23:2380-2384.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 38]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
11.  Canin-Endres J, Salky B, Gattorno F, Edye M. Laparoscopically assisted intestinal resection in 88 patients with Crohn’s disease. Surg Endosc. 1999;13:595-599.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Marcello PW. Laparoscopy for inflammatory bowel disease: pushing the envelope. Clin Colon Rectal Surg. 2006;19:26-32.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 8]  [Cited by in F6Publishing: 7]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
13.  Milsom JW. Laparoscopic surgery in the treatment of Crohn’s disease. Surg Clin North Am. 2005;85:25-34; vii.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 36]  [Article Influence: 1.9]  [Reference Citation Analysis (0)]
14.  Milsom JW, Hammerhofer KA, Böhm B, Marcello P, Elson P, Fazio VW. Prospective, randomized trial comparing laparoscopic vs. conventional surgery for refractory ileocolic Crohn’s disease. Dis Colon Rectum. 2001;44:1-8; discussion 8-9.  [PubMed]  [DOI]  [Cited in This Article: ]
15.  Eshuis EJ, Slors JF, Stokkers PC, Sprangers MA, Ubbink DT, Cuesta MA, Pierik EG, Bemelman WA. Long-term outcomes following laparoscopically assisted versus open ileocolic resection for Crohn’s disease. Br J Surg. 2010;97:563-568.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 114]  [Cited by in F6Publishing: 122]  [Article Influence: 8.7]  [Reference Citation Analysis (0)]
16.  Tilney HS, Constantinides VA, Heriot AG, Nicolaou M, Athanasiou T, Ziprin P, Darzi AW, Tekkis PP. Comparison of laparoscopic and open ileocecal resection for Crohn’s disease: a metaanalysis. Surg Endosc. 2006;20:1036-1044.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 144]  [Cited by in F6Publishing: 119]  [Article Influence: 6.6]  [Reference Citation Analysis (0)]
17.  Huilgol RL, Wright CM, Solomon MJ. Laparoscopic versus open ileocolic resection for Crohn’s disease. J Laparoendosc Adv Surg Tech A. 2004;14:61-65.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 33]  [Cited by in F6Publishing: 38]  [Article Influence: 1.9]  [Reference Citation Analysis (0)]
18.  Bergamaschi R, Pessaux P, Arnaud JP. Comparison of conventional and laparoscopic ileocolic resection for Crohn’s disease. Dis Colon Rectum. 2003;46:1129-1133.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Polle SW, Wind J, Ubbink DT, Hommes DW, Gouma DJ, Bemelman WA. Short-term outcomes after laparoscopic ileocolic resection for Crohn’s disease. A systematic review. Dig Surg. 2006;23:346-357.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 42]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
20.  Bemelman WA, Slors JF, Dunker MS, van Hogezand RA, van Deventer SJ, Ringers J, Griffioen G, Gouma DJ. Laparoscopic-assisted vs. open ileocolic resection for Crohn’s disease. A comparative study. Surg Endosc. 2000;14:721-725.  [PubMed]  [DOI]  [Cited in This Article: ]
21.  Lee Y, Fleming FJ, Deeb AP, Gunzler D, Messing S, Monson JR. A laparoscopic approach reduces short-term complications and length of stay following ileocolic resection in Crohn’s disease: an analysis of outcomes from the NSQIP database. Colorectal Dis. 2012;14:572-577.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 64]  [Cited by in F6Publishing: 66]  [Article Influence: 5.5]  [Reference Citation Analysis (0)]
22.  Lowney JK, Dietz DW, Birnbaum EH, Kodner IJ, Mutch MG, Fleshman JW. Is there any difference in recurrence rates in laparoscopic ileocolic resection for Crohn’s disease compared with conventional surgery? A long-term, follow-up study. Dis Colon Rectum. 2006;49:58-63.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 90]  [Cited by in F6Publishing: 95]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
23.  Stocchi L, Milsom JW, Fazio VW. Long-term outcomes of laparoscopic versus open ileocolic resection for Crohn’s disease: follow-up of a prospective randomized trial. Surgery. 2008;144:622-627; discussion 622-627.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 101]  [Cited by in F6Publishing: 80]  [Article Influence: 5.0]  [Reference Citation Analysis (0)]
24.  Maggiori L, Panis Y. Laparoscopy in Crohn’s disease. Best Pract Res Clin Gastroenterol. 2014;28:183-194.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 13]  [Cited by in F6Publishing: 15]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
25.  da Luz Moreira A, Stocchi L, Remzi FH, Geisler D, Hammel J, Fazio VW. Laparoscopic surgery for patients with Crohn’s colitis: a case-matched study. J Gastrointest Surg. 2007;11:1529-1533.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 37]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
26.  Holubar SD, Dozois EJ, Privitera A, Pemberton JH, Cima RR, Larson DW. Minimally invasive colectomy for Crohn’s colitis: a single institution experience. Inflamm Bowel Dis. 2010;16:1940-1946.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 32]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
27.  Umanskiy K, Malhotra G, Chase A, Rubin MA, Hurst RD, Fichera A. Laparoscopic colectomy for Crohn’s colitis. A large prospective comparative study. J Gastrointest Surg. 2010;14:658-663.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 33]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]
28.  Regan JP, Salky BA. Laparoscopic treatment of enteric fistulas. Surg Endosc. 2004;18:252-254.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 29]  [Article Influence: 1.4]  [Reference Citation Analysis (0)]
29.  Alves A, Panis Y, Bouhnik Y, Marceau C, Rouach Y, Lavergne-Slove A, Vicaut E, Valleur P. Factors that predict conversion in 69 consecutive patients undergoing laparoscopic ileocecal resection for Crohn’s disease: a prospective study. Dis Colon Rectum. 2005;48:2302-2308.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 81]  [Cited by in F6Publishing: 66]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
30.  Dignass A, Van Assche G, Lindsay JO, Lémann M, Söderholm J, Colombel JF, Danese S, D’Hoore A, Gassull M, Gomollón F. The second European evidence-based Consensus on the diagnosis and management of Crohn’s disease: Current management. J Crohns Colitis. 2010;4:28-62.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1043]  [Cited by in F6Publishing: 1011]  [Article Influence: 72.2]  [Reference Citation Analysis (1)]
31.  Beyer-Berjot L, Mancini J, Bege T, Moutardier V, Brunet C, Grimaud JC, Berdah S. Laparoscopic approach is feasible in Crohn’s complex enterovisceral fistulas: a case-match review. Dis Colon Rectum. 2013;56:191-197.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 23]  [Cited by in F6Publishing: 23]  [Article Influence: 2.1]  [Reference Citation Analysis (0)]
32.  Goyer P, Alves A, Bretagnol F, Bouhnik Y, Valleur P, Panis Y. Impact of complex Crohn’s disease on the outcome of laparoscopic ileocecal resection: a comparative clinical study in 124 patients. Dis Colon Rectum. 2009;52:205-210.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 108]  [Cited by in F6Publishing: 96]  [Article Influence: 6.4]  [Reference Citation Analysis (0)]
33.  Brouquet A, Bretagnol F, Soprani A, Valleur P, Bouhnik Y, Panis Y. A laparoscopic approach to iterative ileocolonic resection for the recurrence of Crohn’s disease. Surg Endosc. 2010;24:879-887.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 41]  [Cited by in F6Publishing: 47]  [Article Influence: 3.4]  [Reference Citation Analysis (0)]
34.  Chaudhary B, Glancy D, Dixon AR. Laparoscopic surgery for recurrent ileocolic Crohn’s disease is as safe and effective as primary resection. Colorectal Dis. 2011;13:1413-1416.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 39]  [Cited by in F6Publishing: 42]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
35.  Moorthy K, Shaul T, Foley RJ. Factors that predict conversion in patients undergoing laparoscopic surgery for Crohn’s disease. Am J Surg. 2004;187:47-51.  [PubMed]  [DOI]  [Cited in This Article: ]
36.  Aytac E, Stocchi L, Remzi FH, Kiran RP. Is laparoscopic surgery for recurrent Crohn’s disease beneficial in patients with previous primary resection through midline laparotomy? A case-matched study. Surg Endosc. 2012;26:3552-3556.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 30]  [Cited by in F6Publishing: 31]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
37.  Gardenbroek TJ, Verlaan T, Tanis PJ, Ponsioen CY, D’Haens GR, Buskens CJ, Bemelman WA. Single-port versus multiport laparoscopic ileocecal resection for Crohn’s disease. J Crohns Colitis. 2013;7:e443-e448.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 24]  [Cited by in F6Publishing: 25]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
38.  Rijcken E, Mennigen R, Argyris I, Senninger N, Bruewer M. Single-incision laparoscopic surgery for ileocolic resection in Crohn’s disease. Dis Colon Rectum. 2012;55:140-146.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 58]  [Article Influence: 4.8]  [Reference Citation Analysis (0)]
39.  Maeda K, Noda E, Nagahara H, Inoue T, Takii M, Watanabe K, Yamagami H, Sogawa M, Kamata N, Hirakawa K. A comparative study of single-incision versus conventional multiport laparoscopic ileocecal resection for Crohn’s disease with strictures. Asian J Endosc Surg. 2012;5:118-122.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 19]  [Cited by in F6Publishing: 21]  [Article Influence: 1.8]  [Reference Citation Analysis (0)]
40.  Cohen RD, Larson LR, Roth JM, Becker RV, Mummert LL. The cost of hospitalization in Crohn’s disease. Am J Gastroenterol. 2000;95:524-530.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 111]  [Cited by in F6Publishing: 119]  [Article Influence: 5.0]  [Reference Citation Analysis (0)]
41.  Yu AP, Cabanilla LA, Wu EQ, Mulani PM, Chao J. The costs of Crohn’s disease in the United States and other Western countries: a systematic review. Curr Med Res Opin. 2008;24:319-328.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 144]  [Cited by in F6Publishing: 197]  [Article Influence: 12.3]  [Reference Citation Analysis (0)]
42.  Feagan BG, Vreeland MG, Larson LR, Bala MV. Annual cost of care for Crohn’s disease: a payor perspective. Am J Gastroenterol. 2000;95:1955-1960.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 138]  [Cited by in F6Publishing: 146]  [Article Influence: 6.1]  [Reference Citation Analysis (0)]
43.  Keller DS, Katz J, Stein SL, Delaney CP. Surgical cost of care in Crohn’s disease. Pol Przegl Chir. 2013;85:511-516.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 3]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
44.  Lesperance K, Martin MJ, Lehmann R, Brounts L, Steele SR. National trends and outcomes for the surgical therapy of ileocolonic Crohn’s disease: a population-based analysis of laparoscopic vs. open approaches. J Gastrointest Surg. 2009;13:1251-1259.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 71]  [Cited by in F6Publishing: 69]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
45.  Jensen CC, Prasad LM, Abcarian H. Cost-effectiveness of laparoscopic vs open resection for colon and rectal cancer. Dis Colon Rectum. 2012;55:1017-1023.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 47]  [Cited by in F6Publishing: 46]  [Article Influence: 3.8]  [Reference Citation Analysis (0)]
46.  Moftah M, Nazour F, Cunningham M, Cahill RA. Single port laparoscopic surgery for patients with complex and recurrent Crohn’s disease. J Crohns Colitis. 2014;Feb 28; Epub ahead of print.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 25]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]