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Laparoscopic resection for primary and recurrent Crohn's disease: A case series of over 100 consecutive cases
International Journal of Surgery 47 (2017) 69e76
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Original Research
Laparoscopic resection for primary and recurrent Crohn's disease: A case series of over 100 consecutive cases Sofoklis Panteleimonitis a, b, *, Jamil Ahmed a, Thomas Parker a, Tahseen Qureshi a, c, Amjad Parvaiz a, b, d a
Poole Hospital NHS Trust, Longfleet Road, Poole, United Kingdom University of Portsmouth, School of Health Sciences and Social Work, Portsmouth, United Kingdom Bournemouth University School of Health and Social Care, Bournemouth, United Kingdom d Champalimaud Foundation, Lisbon, Portugal b c
h i g h l i g h t s Laparoscopic resection surgery for Crohn's disease is safe and feasible. In the hands of experienced laparoscopic surgeons conversion rates are minimal (4.7% in our series). Laparoscopic surgery is a viable option for patients having recurrent or emergency resection surgery for Crohn's disease.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 May 2017 Received in revised form 13 September 2017 Accepted 16 September 2017 Available online 22 September 2017
Background: Laparoscopic surgery for patients with Crohn's disease (CD) is considered challenging. The aim of this study is to evaluate the clinical outcomes of laparoscopic bowel resection in patients with CD. We also assessed the effectiveness of the laparoscopic approach in recurrent or emergency surgery due to CD. Materials and methods: All patients with CD, who underwent laparoscopic resection surgery in two units from October 2006 to February 2016, were identified through prospectively maintained databases. Their baseline characteristics and perioperative outcomes were analysed. The outcomes of patients receiving primary vs recurrent and elective vs emergency laparoscopic resections for CD were also examined. Results: In total 106 patients underwent laparoscopic resection. Primary ileocolic resection was the most frequent procedure (62%) followed by redo-ileocolic resection (15%). Overall conversion rate was 4.7%, median operative time was 130 (95e185) minutes and length of stay was 4 days (3e6). There was one anastomotic leak (1.1%) and 30-day re-operation rate was 5.7%. Patients having primary resections were younger and had a shorter length of stay (4 vs 5 days; p ¼ 0.014). Thirty day re-operation rate was higher in patients having emergency surgery (3.1% vs 30%; p ¼ 0.011). Conclusions: This case series demonstrates that laparoscopic resection surgery for CD is safe and feasible. Similarly, laparoscopic surgery is also a viable option for patients having recurrent resection and possibly even emergency surgery. Crown Copyright © 2017 Published by Elsevier Ltd on behalf of IJS Publishing Group Ltd. All rights reserved.
Keywords: Crohn's disease Laparoscopy Colorectal surgery
1. Introduction Despite advances in the medical management of Crohn's disease
* Corresponding author. University of Portsmouth, School of Health Sciences and Social Work, James Watson West, 2 King Richard 1st Road, Portsmouth, PO1 2FR, United Kingdom. E-mail address: [email protected] (S. Panteleimonitis).
(CD) the majority of Crohn's patients will undergo surgical treatment during their lifetime [1e6]. In addition, 40e50% of patients that receive surgical treatment for Crohn's will require further surgery within the next 10e15 years [6e10]. Laparoscopy has become the gold standard throughout the developed world for the majority of gastrointestinal procedures [10,11]. However, Crohn's patients are often considered poor candidates for laparoscopic surgery due to the nature of the disease. It often involves extensive
https://doi.org/10.1016/j.ijsu.2017.09.055 1743-9191/Crown Copyright © 2017 Published by Elsevier Ltd on behalf of IJS Publishing Group Ltd. All rights reserved.
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inflammation, thickened mesentery, skip lesions throughout the bowel and enteric fistulae [12]. Despite the challenges of laparoscopic surgery in patients with CD, Crohn's patients have potentially a lot to gain from this approach. Considering their young age and frequent need for repeated operations the benefits of improved cosmesis, less postoperative pain, shorter length of stay, earlier return to work, reduced adhesional formation and reduced incidence of incisional hernias due to the conservation of abdominal wall integrity are undeniably appealing [1,13,14]. These benefits have led to many laparoscopic surgeons to adopt a minimally invasive approach for patients with CD over the last two decades and it is now feasible to perform the whole range of CD interventions laparoscopically [2]. There are a number of case series describing laparoscopy in patients with CD [12,15e17]. Studies have also shown that the laparoscopic approach has better short and long-term outcomes when compared to open surgery [1,18e22]. The objectives of this study are to investigate the safety and feasibility of laparoscopic bowel resection for CD and assess its feasibility for recurrent and emergency CD surgery. To achieve this we describe the peri-operative and short term outcomes of patients receiving laparoscopic resection surgery for CD from two centres in the United Kingdom over the last 9 years. We also compare the outcomes of primary laparoscopic resections with redo laparoscopic resections for recurrent disease and the outcomes of laparoscopic resections in an elective vs emergency setting. To our knowledge, this is the largest series of laparoscopic bowel resections for CD in the UK to date. 2. Materials and methods All patients with CD, who underwent laparoscopic surgery in two National Health Service (NHS) units in the UK from October 2006 to February 2016, were identified through prospectively maintained databases. Patients undergoing primary, redo, elective and emergency laparoscopic resections were included in the analysis. Inclusion criteria were: all patients receiving laparoscopic bowel resection surgery for CD. Exclusion criteria were: non-bowel resection surgery (e.g. stricturoplasty), open surgery and surgery for ulcerative colitis or cancer. Two experienced laparoscopic colorectal surgeons performed or closely supervised all procedures in each unit. Both surgeons had vast experience in laparoscopic colorectal benign and malignant surgery and both surgeons were trainers for the LAPCO training programme, the UK's national training programme for laparoscopic colorectal surgery [23]. Surgeon A was the senior surgeon who trained surgeon B, hence both surgeons applied the same standardised modular approach to surgery [24] and peri-operative care regime. Informed consent was obtained from all patients. Appropriate approval for the study was obtained by Poole Hospital NHS Trust. The study was registered with ResearchRegitry.com (Unique Identification Number: researchregistry2518) and the research work has been reported in line with the PROCESS criteria [25]. Data was collected prospectively and analysed for baseline characteristics, peri-operative data and short term post-operative data. Conversion was defined as any incision needed to either mobilise the specimen or ligate the vessels. For a procedure to be considered laparoscopically completed there should be no conversion as defined above. Converted patients were included in the analysis as we performed an intention to treat analysis. 2.1. Peri-operative care Pre-operative workup included computer tomography (CT) and or magnetic resonance imaging (MRI) enteroclysis, ultrasound
examinations and colonoscopy to exclude or assess colonic disease. Laparoscopy was the default approach for all patients with surgeries either performed or closely supervised by the consultant surgeons, with the consultant surgeon always scrubbed for all cases. The only contra-indication to laparoscopy was patients not deemed anaesthetically fit to tolerate pneumoperitoneum. However, one should note that these patients are rarely fit for open surgery either. Patients with complex problems were discussed at the inflammatory bowel disease multidisciplinary team meeting (IBD MDT) and referred for resection if deemed necessary. Indications for surgery included: failure of medical management, fistulating disease, obstructing stricture and abdominal sepsis due to perforation, abscess or mass. Post-operative care was standardised, with patients entering a routine enhanced recovery programme and receiving follow up from a multi-disciplinary team of health care professionals including the colorectal team, the gastroenterologists, the nutrition team and the stoma nurses. Antibiotics were only given routinely on induction, where a single intravenous dose of 1.5gr cefuroxime and 500 mg metronidazole was given. A single shot spinal infiltration containing a mixture of diamorphine and marcaine was given prior to anaesthesia for analgesia, no epidural catheters were used and wounds were infiltrated with local anaesthetic. After surgery patients were encouraged to drink fluids on the same evening, get out of bed as soon as possible and eat solids as soon they felt to and once oral fluids were tolerated. Intravenous hydration was removed as soon as the patient could tolerate oral fluids, urinary catheters were taken out the morning after surgery and analgesia was carried out with oral paracetamol and ibuprofen. All patients undergoing emergency or urgent resections were on immunosuppressive medication and could not be taken off this medication prior to surgery. Patients receiving elective surgery had their immunosuppressive medication tapered off and stopped four weeks prior to surgery. All patients having emergency resections had poor nutritional statuses while elective patients were nutritionally optimised and had a normal nutritional status; defined as a serum albumin level that was over 30 gr/liter.
2.2. Operative technique All procedures were performed through a well-established standardised modular technique [24]. This approach permits a safe and reproducible technique that also facilitates teaching and training [24]. Since most of the procedures performed were ileocolic resections, we describe its operative technique as below. The patient was placed in the modified Lloyd Davies position. The optical port was placed infra umbilical in the midline with the open Hassan technique and pneumoperitoneum was established. In case of a previous midline scar, open technique for insufflation was performed in the left upper abdomen. Pressure was set to 12 mmHg. Further ports were inserted under direct vision and placement is described in Fig. 1. For the initial setting the patient was placed in the reversed Trendelenburg position with the left sided tilted down. The omentum was retracted cranially over the upper compartment and the transverse colon was exposed. The small bowel was moved to the left side to expose the duodenal area. Surgical dissection is divided into the following steps: 1 2 3 4
Vessel Control with medial to lateral dissection Sub-ileal dissection Lateral Mobilization Hepatic Flexure Mobilization (if required)
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Table 1 Baseline characteristics of patients with Crohn's disease. Total (n ¼ 106) Sex Male Female Median age (IQRa) Mean BMI (SDb) ASA grade I II III IV Surgeon A B Urgency Elective Emergency a b
48 (45.3%) 58 (54.7%) 40 (29e52.25) 23.8 (4.16) 12 75 13 1 65 41 96 (90.6%) 10 (9.4%)
IQR: Inter-quartile range. SD: standard deviation.
previous abdominal surgery. Of those 19 had received previous resectional surgery for CD, including 18 ileocolic resections and one anterior resection. The remaining patients having previous abdominal surgery included four appendicectomies, one laparotomy, three ileostomies, two hysterectomies and a Caesarean. All previous abdominal surgeries were open procedures. 3.2. Operative outcomes Fig. 1. Port placement for ileocolic resection.
5 Specimen extraction and extracorporeal side-to-side stapled/ mechanical anastomosis using a TLC75 ETHICON PROXIMATE® Linear Cutter stapler During early experience a 10 mm LigaSure Atlas™ Covidien energy device was used to seal the thick mesentery. Subsequently, when the 5 mm LigaSure device became available we routinely performed procedures using this energy source to seal and divide the mesentry. Vessels were isolated and ligated with haem-olocks™. Vessel control was always done laparoscopically. The usual extraction site was in the midline at the peri-umbilical port site. A transverse incision in the right side of the abdomen was avoided as it could be used for future stoma formation. At the end of the procedure a check laparoscopy was performed to look for haemostasis. Drains and nasogastric tubes were avoided. 2.3. Statistics methods IBM SPSS version 22 (SPSS Inc., Chicago, IL, USA) and Microsoft Excel 2010™ were used for the statistical analysis. Data was expressed as median with interquartile range for non-parametric data and mean with standard deviation for parametric data. Clinical characteristics were compared using c2 test or Fishers exact test for categorical variables and Mann-Whitney U test (nonparametric) and t-test (parametric) for continuous variables. 3. Results 3.1. Demographics One hundred and six patients underwent laparoscopic surgery for CD between October 2006 and February 2016. Their baseline characteristics are shown in Table 1. Thirty (28.3%) patients had
Primary ilieocolic resection was the most frequent procedure, 62.3% (n ¼ 66), followed by redo-ileocolic resection, 15.1% (n ¼ 16). There were 3 small bowel resections, with the remaining procedures being colonic resections: 7 panproctocolectomies, 6 subtotal colectomies, 4 proctocolectomies, 2 sigmoid colectomies, 1 abdominoperineal resection and 1 right and sigmoid colectomy. Fig. 2 provides a patient flowchart of the procedures performed, dividing them in primary vs recurrent, emergency vs elective and stating which procedures required re-operations. Five procedures were converted to open (4.7% conversion rate). Median operative time was 130 min (95e185) and median blood loss 20 mls (0e50). The operative outcomes are summarised on Table 2. 3.3. Post-operative outcomes The details of post-operative outcomes are illustrated in Table 2. Median length of stay was 4 days (3e6). Thirty day re-operation rate was 5.7% (n ¼ 6). Regarding those, five of them were following primary ileocolic resections and half of them (n ¼ 3) were following emergency surgery. One of them was done for an anastomotic leak, two were done secondary to small bowel obstruction, two were done for suspected sepsis with subsequent normal intraoperative findings and one was an evacuation of a haematoma. There were 18 (17%) 30-day readmissions; these were due to a variety of reasons including 5 patients readmitted with nausea and vomiting, 4 with non-specific abdominal pain, 2 with a wound infection, a patient with an infected haematoma that was treated with antibiotics, a patient with a subhepatic collection that was treated conservatively, a patient admitted with acute kidney injury and small bowel obstruction that settled with conservative measures, a patient with ileus and haematoma that developed a subsequent pulmonary embolus during readmission, two patients with small bowel obstruction and one with an anastomotic leak. The latter 4 patients required surgery during their readmission and are
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Fig. 2. Patient flowchart.
Table 2 Peri-operative and short term post-operative outcomes of patients with Crohn's disease. Total (n ¼ 106) Conversion to open Median operative time in minutes (IQRa) Median blood loss in mls (IQR) Median length of stay in days (IQR) 30-day readmissions 30-day re-operations Anastomotic leaks 30-day mortality a
5 (4.7%) 130 (95e185) 20 (0e50) 4 (3e6) 18 (17.0%) 6 (5.7%) 1 (1.1%) 0
IQR: Inter-quartile range.
included in the 30-day re-operation group (Clavien-Dindo 3b). The
remaining of the readmissions were grade 1e2 in the ClavienDindo scale. Regarding the patient with the anastomotic leak, he presented on day 6 post-op with a right upper quadrant abscess (collection). It is difficult to pin point the exact cause of the leak although there was no obvious bowel ischaemia.
3.4. Primary vs recurrent resections The outcomes of patients undergoing primary resections vs redo resections for CD are presented in Table 3. The primary group consisted of 66 ileocolic resections, two small bowel resections and 19 colonic resections while the recurrent group consisted of 16 redo-ileocolic resections, one small bowel resection and 2 colonic resections.
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Table 3 Baseline characteristics and surgical outcomes of primary vs recurrent resections for Crohn's disease.
Median age (IQRa) Mean BMI (SDb) Conversion rate Median operation time (min) Median blood loss (mls) Median length of stay (days) 30-day readmission rate 30-day re-operation rate Anastomotic leak rate
Primary resection (n ¼ 87)
Recurrent (n ¼ 19)
P value
36 (28e49) 23.6 (4.01) 4 (4.6%) 127.5 (90e183.75) 20 (0e50) 4 (3e6) 13 (14.9%) 6 (6.9%) 1 (1.4%)
48 (42e68) 25 (4.83) 1 (5.3%) 145 (123.75e185.75) 20 (10e50) 5 (4.25e7.75) 5 (26.3%) 0 0
0.001m 0.228t 1.000f 0.147m 0.661m 0.014m 0.309f 0.589f 1.000f
m: Mann-Whitney U. t: t-test. f: Fischer's exact test. a IQR: Inter-quartile range. b SD: standard deviation.
There was no difference in the conversion rate between patients having primary or recurrent surgery for CD (4.6% vs 5.3%; p ¼ 1.000). None of the converted patients having primary surgery for CD had any other form of previous abdominal surgery. Patients having primary resections tended to be younger than those having recurrent resection surgery (p ¼ 0.001). Apart from length of stay, which was one day longer in patients undergoing recurrent resections (4 vs 5 days; p ¼ 0.014), there was no statistical difference in any of the other short-term surgical outcomes. 3.5. Elective vs emergency resections The outcomes of patients undergoing elective and emergency laparoscopic resection surgery for CD are summarized is Table 4. The elective group consisted of 58 ileocolic resections, 16 redoileocolic resections, 3 small bowel resections and 19 colonic resections while the emergency group consisted of 8 ileocolic resections and 2 colonic resections. Thirty day re-operation rate was higher in patients having emergency surgery (3.1% vs 30%; p ¼ 0.011). Length of stay appeared to be longer in the emergency group but this did not reach statistical significance (4 vs 8 days, p ¼ 0.115). There were no statistically significant differences in any of the other outcomes between the two groups. 4. Discussion This study shows that laparoscopic surgery is feasible with a low conversion rate, acceptable operative time, minimal blood loss and
good post-operative outcomes. Furthermore, this case series also demonstrates that disease recurrence and an emergency setting (in haemodynamically stable patients) are not contraindications for laparoscopic surgery. The majority of patients requiring resection surgery for CD underwent ileocolic resections. This is in accordance with the prevalence of the disease, which tends to predominantly affect the terminal ileum [10,12]. The conversion rate was 4.7%, which includes all patients undergoing resection surgery for CD. This is despite 28.3% of patients induced in this study having received previous open abdominal surgery. Our conversion rate supports the feasibility of laparoscopic surgery in CD and is in accordance with the published evidence, in which conversion rate varies between 2% and 42% for patients with CD [12,20,22,26,27]. The variation found in the literature is probably due to differences in defining a conversion to open, variability in laparoscopic experience among the operating surgeons, disease severity and site of affected segment [26,28e30]. It is worth noting that a recent study by Masoomi et al. examining the American National Inpatient Sample (NIS) database reported a conversion rate for patient's receiving laparoscopic surgery for CD of 20% and concluded that Crohn's is a strong predictor for conversion in laparoscopic surgery [31]. This is in contrast to our findings and those of other published reports [1,2,12,22,32], where conversion rates were comparable to that of laparoscopic colorectal oncological surgery. The most likely explanation for this difference is the variability of laparoscopic experience of the performing surgeons. The NIS database includes a huge cohort of surgeons with variable laparoscopic experience. In contrast, the conversion rate reported by Nguyen et al. [12] in 335
Table 4 Baseline characteristics and surgical outcomes of elective vs emergency surgery for Crohn's disease.
Median age (IQRa) Mean BMI (SDb) Conversion rate Median operation time (min) Median blood loss (mls) Median length of stay (days) 30-day readmission rate 30-day re-operation rate Anastomotic leak rate m: Mann-Whitney U. t: t-test. f: Fischer's exact test. Bold value signifies p < 0.05. a IQR: Inter-quartile range. b SD: standard deviation.
Elective resections (n ¼ 96)
Emergency (n ¼ 10)
P value
40.5 (30.25e52.75) 24 (4.19) 4 (4.2%) 130 (95e182.5) 20 (0e50) 4 (3e6) 16 (16.7%) 3 (3.1%) 1 (1.3%)
35 (23.5e53.75) 21.6 (3.26) 1 (10%) 120 (92.5e200) 20 (0e35) 8 (3e18.5) 2 (20%) 3 (30%) 0
0.479m 0.139t 0.397f 0.953m 0.506m 0.115m 0.677f 0.011f 1.000f
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cases of laparoscopic resections for CD is only 2%. In this study the procedures were performed by surgeons with vast laparoscopic experience in a tertiary centre for CD. Equally, in our cohort all procedures were performed by experienced laparoscopic surgeons, which accounts for our low conversion rate. Median operative time in our study was 130 min for all resections, 127.5 min in primary resections and 145 min in patients with recurrent disease. Operative time is variable across the literature, ranging between 85 and 185 min for first ileocolic resection [7,15,16,20,32,33] and 118e215 min for recurrent ileocolic resections [15,16,29,34]. In our study, operative time appeared shorter in patients receiving primary resections compared to those with recurrent disease (Table 3), but this did not reach statistical significance. Previous studies have reported contradictory results, with some demonstrating shorter operative times in primary laparoscopic Crohn's resections when compared to recurrent resections [7,16], with other studies reporting no difference [15,35]. The post-operative outcomes of this study reinforce the acumen that laparoscopic surgery is safe and feasible in the hands of surgeons with appropriate laparoscopic experience. The median length of stay was 4 days, while in previous studies the length of stay tends to range between 5 and 7 days in primary resections [18e20,32,36] and up to 9 days in recurrent ones [2,15,16,29,34]. Thirty day readmission rate, reoperation rate and overall anastomotic leak rate were acceptable in our cohort (Table 2), further demonstrating the feasibility of the laparoscopic approach for this type of surgery. Previous evidence comparing anastomotic leak rate and morbidity of open vs laparoscopic Crohn's surgery after first ileocolic resection supports this, with studies showing similar outcomes [10,20,22,33] or outcomes favouring the laparoscopic approach [18,19]. It is important to note that all patients entered an enhanced recovery after surgery programme (ERAS), which has a major role in the post-operative outcomes presented. It is hard to know in what degree the post-operative outcomes presented are due to laparoscopy or the ERAS programme. The majority of our patients that were readmitted were due to Clavien-Dindo grade 1e2 complications, with only 4 (22%) being readmitted with grade 3 complications or above. The commonest causes were non-specific abdominal pain and nausea and vomiting. Even though no formal diagnosis was given for these patients they all settled with conservative measures (Clavien-Dido grade 1). Comparison of the outcomes of patients having laparoscopic surgery for primary vs recurrent resections showed that patients having primary resections tend to be younger and have a shorter length of stay (Table 3). Patients requiring recurrent resection surgery tend to be older since they have already had their primary surgery earlier in their lives. Patients requiring recurrent resection surgery for Crohn's can be sicker and their surgery is often more technically demanding. This might explain why patients in the recurrent cohort stayed in hospital an extra day. Nevertheless, this was not reflected in any of the other peri- and post-operative outcomes and although median operation time and 30-day readmission rate were also higher in the recurrent cohort, they were not statistically significant (Table 3). These results are in accordance with previously published reports that have shown similar postoperative outcomes for patients receiving surgery for primary vs recurrent disease [15,16]. Furthermore, conversion rate was similar between the two groups. One might have expected to find a higher conversion rate in surgery for recurrent disease, due to the formation of adhesions. However, the majority of the evidence dismisses that [7,15,16] as does our study (Table 3). Patients having emergency surgery for CD had a higher 30-day re-operation rate (Table 4). This is probably a reflection of the poor physiological state of these patients, which are usually acutely unwell and have been on high dose of immunosuppressive agents.
This is contrast to patients receiving elective surgery who have been tapered off their immunosuppressive medication and are in a nutritionally acceptable status. This can explain why patients in the emergency cohort stayed in hospital twice as long (4 vs 8 days), although this did not reach statistical significance due to the small number of cases in the emergency group (n ¼ 10). It should be noted that although the re-operation rate was higher in the emergency group, there were only three re-operations. One of them was an evacuation of a haematoma and two were laparoscopies, one of which was negative (see Fig. 2). Considering the small number of emergency patients in this study these results need to be taken into account with caution. Moreover, in this series all patients operated on an emergency setting were haemodynamically stable and only patients deemed by the anaesthetist as fit enough to tolerate a pneumoperitoneum received laparoscopic surgery. Therefore, the conclusions derived regarding emergency patients in this study only apply for stable patients. So far the published evidence for emergency laparoscopic surgery for CD is mainly limited to case reports as its application is still on debate [37,38]. However, since laparoscopy for abdominal surgical emergencies is gaining increasing acceptance it is likely that laparoscopic emergency surgery for CD will become more common. In this study three patients were operated on because of fistulating disease and two because of intra-abdominal abscesses. It is worth noting that despite the pathology of these patients, they were all operated on in an elective setting, none of them had an anastomotic leak and none of them were readmitted or re-operated on within 30 days. We acknowledge the limitations of this study, being retrospective in nature and essentially a description of a case series. In addition, we have not reported minor post-operative complications (Clavien-Dindo 1e2). This is because on our data set we only record complications that result in re-operation, re-intervention (ClavienDindo grade 3 or more) or complications resulting in a readmission. It is conceivable that minor complications (Clavien-Dindo 1e2) would be reflected in prolonged hospital stay which was not the case for our study. Another limitation might be that the experience of the two surgeons might not be reflective of the much wider cohort of surgeons performing laparoscopic colorectal surgery. Regardless, considering our large sample size and study design, we believe our study has enough power to demonstrate the feasibility of laparoscopic Crohn's surgery in the hands of experienced laparoscopic surgeons where operative technique and post-operative treatment have been standardised. Furthermore, the majority of the current evidence in this topic is based on non-randomised, retrospective studies with small sample size numbers. Findings throughout the literature seem to consistently support the feasibility of laparoscopy for CD. Even though larger scale randomised control trials comparing laparoscopic vs open surgery would be desirable in order to obtain concrete evidence [3], considering the amount of current evidence one could debate that performing such a study on this group of relatively young and slim patients might be against the patients best interests. 5. Conclusions In summary, this study has shown that laparoscopic resection surgery for CD is safe and feasible when operative technique and post-operative care has been standardised in the hands of experienced laparoscopic colorectal surgeons. Furthermore, this study demonstrated that laparoscopic surgery is a viable option for patients with recurrent disease and possibly even those undergoing emergency surgery, if haemodynamically stable. Considering the majority of the previous studies examining the feasibility of laparoscopic surgery for CD have small sample sizes
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this study enriches the available literature since it presents the largest case series in the UK so far. In addition, it is unique since it compares the outcomes of both primary vs recurrent and elective vs emergency laparoscopic CD resection surgery. Further larger scale multicentre case series are needed to solidify the feasibility and safety of laparoscopy for CD. Ethical approval Ethical approval was not required since the study is a retrospective case series with no patient identifiable data. According to the Health Research Authority (HRA), this study was not classified to need their approval. The study was approved by Poole Hospital NHS Trust. Funding No funding was obtained in order to perform or write up this study. Author contribution Conception and design: Sofoklis Panteleimonitis, Amjad Parvaiz. Analysis and interpretation of the data: Sofoklis Panteleimonitis, Thomas Parker. Drafting of the article: Sofoklis Panteleimonitis. Critical revision of the article for important intellectual content: Jamil Ahmed, Amjad Parvaiz, Tahseen Qureshi. Final approval of the article: Amjad Parvaiz, Tahseen Qureshi. Conflict of interest No conflicts of interest to declare by any of the authors. Research Registration Unique Identifying Number (UIN) The study was registered with ResearchRegistry.com. The Unique Identification Number is researchregistry2518. Guarantor Sofoklis Panteleimonitis. Professor Amjad Parvaiz. Acknowledgement We thank Karen Flashman for her hard work on maintaining the surgical database on daily basis. References [1] J.Y. Lim, J. Kim, S.Q. Nguyen, Laparoscopic surgery in the management of Crohn's disease, World J. Gastrointest. Pathophysiol. 5 (2014) 200e204, https://doi.org/10.4291/wjgp.v5.i3.200. [2] M. Tavernier, G. Lebreton, a Alves, Laparoscopic surgery for complex Crohn's disease, J. Visc. Surg. 150 (2013) 389e393, https://doi.org/10.1016/ j.jviscsurg.2013.09.004. [3] S. V Patel, S.V.B. Patel, S. V Ramagopalan, M.C. Ott, Laparoscopic surgery for Crohn's disease: a meta-analysis of perioperative complications and long term outcomes compared with open surgery, BMC Surg. 13 (2013) 14, https:// doi.org/10.1186/1471-2482-13-14. [4] R.D. Cohen, J.F. Tsang, S.B. Hanauer, Infliximab in Crohn's disease: first anniversary clinical experience, Am. J. Gastroenterol. 95 (2000) 3469e3477, https://doi.org/10.1111/j.1572-0241.2000.03363.x. [5] V. Binder, H. Both, P.K. Hansen, C. Hendriksen, S. Kreiner, K. Torp-Pedersen, Incidence and prevalence of ulcerative colitis and Crohn's disease in the County of Copenhagen, 1962 to 1978, Gastroenterology 83 (1982) 563e568. [6] O. Bernell, A. Lapidus, G. Hellers, Risk factors for surgery and recurrence in 907 patients with primary ileocaecal Crohn's disease, Br. J. Surg. 87 (2000)
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Dixon, Laparoscopic surgery for recurrent ileocolic Crohn's disease is as safe and effective as primary resection, Color. Dis. 13 (2011) 1413e1416, https://doi.org/10.1111/j.1463-1318.2010.02511.x. [17] P. Goyer, A. Alves, F. Bretagnol, Y. Bouhnik, P. Valleur, Y. Panis, Impact of complex Crohn's disease on the outcome of laparoscopic ileocecal resection: a comparative clinical study in 124 patients, Dis. Colon Rectum 52 (2009) 205e210, https://doi.org/10.1007/DCR.0b013e31819c9c08. [18] J.W. Milsom, K.A. Hammerhofer, B. Bohm, P. Marcello, P. Elson, V.W. Fazio, Prospective, randomized trial comparing laparoscopic vs. conventional surgery for refractory ileocolic Crohn's disease, Dis. Colon Rectum 44 (2001) 1e9. [19] S. Maartense, M.S. Dunker, J.F.M. Slors, M.A. Cuesta, E.G.J.M. Pierik, D.J. Gouma, D.W. Hommes, M.A. Sprangers, W.A. Bemelman, Laparoscopic-assisted versus open ileocolic resection for Crohn's disease: a randomized trial, Ann. Surg. 243 (2006) 143, https://doi.org/10.1097/01.sla.0000197318.37459.ec. tirich, H. Bedioui, M. Jouini, M. Kacem, [20] a Makni, F. Chebbi, R. Ksantini, F. Fe N. Ben Mami, a. Filali, Z. Ben Safta, Laparoscopic-assisted versus conventional ileocolectomy for primary Crohn's disease: results of a comparative study, J. Visc. Surg. 150 (2013) 137e143, https://doi.org/10.1016/ j.jviscsurg.2012.10.006. [21] A. Fichera, S.L. Peng, N.M. Elisseou, M.a. Rubin, R.D. Hurst, Laparoscopy or conventional open surgery for patients with ileocolonic Crohn's disease? A prospective study, Surgery 142 (2007) 566e571, https://doi.org/10.1016/ j.surg.2007.08.004. [22] H.S. Tilney, V.a. Constantinides, a.G. Heriot, M. Nicolaou, T. Athanasiou, P. Ziprin, a.W. Darzi, P.P. Tekkis, Comparison of laparoscopic and open ileocecal resection for Crohn's disease: a metaanalysis, Surg. Endosc. Other Interv. Tech. 20 (2006) 1036e1044, https://doi.org/10.1007/s00464-005-0500-3. [23] M.G. Coleman, G.B. Hanna, R. Kennedy, The national training programme for laparoscopic colorectal surgery in England: a new training paradigm, Colorectal Dis. 13 (2011) 614e616, https://doi.org/10.1111/j.14631318.2011.02643.x. [24] A. Hemandas, K.G. Flashman, J. Farrow, D.P. O'Leary, A. Parvaiz, Modular training in laparoscopic colorectal surgery maximizes training opportunities without clinical compromise, World J. Surg. 35 (2011) 409e414, https:// doi.org/10.1007/s00268-010-0837-1. [25] R.A. Agha, A.J. Fowler, S. Rajmohan, I. Barai, D.P. Orgill, Preferred reporting of case series in surgery; the PROCESS guidelines, Int. J. Surg. 36 (2016) 319e323, https://doi.org/10.1016/j.ijsu.2016.10.025. [26] J.S. Mino, N.S. Gandhi, L.L. Stocchi, M.E. Baker, X. Liu, F.H. Remzi, R. Monteiro, J.D. Vogel , Preoperative risk factors and radiographic findings predictive of laparoscopic conversion to open procedures in Crohn's disease, J. Gastrointest. Surg. 19 (2015) 1007e1014, https://doi.org/10.1007/s11605-015-2802-7. [27] K. Shigeta, K. Okabayashi, H. Hasegawa, M. Tsuruta, R. Seishima, Y. Kitagawa, Meta-analysis of laparoscopic surgery for recurrent Crohn's disease, Surg. Today (2015), https://doi.org/10.1007/s00595-015-1271-7. [28] A. Alves, Y. Panis, Y. Bouhnik, C. Marceau, Y. Rouach, A. Lavergne-Slove, E. Vicaut, P. Valleur, Factors that predict conversion in 69 consecutive patients undergoing laparoscopic ileocecal resection for Crohn's disease: a prospective study, Dis. Colon Rectum 48 (2005) 2302e2308, https://doi.org/10.1007/ s10350-005-0190-x. [29] A. Brouquet, F. Bretagnol, A. Soprani, P. Valleur, Y. Bouhnik, Y. Panis, A laparoscopic approach to iterative ileocolonic resection for the recurrence of Crohn's disease, Surg. Endosc. 24 (2010) 879e887, https://doi.org/10.1007/ s00464-009-0682-1. [30] T.M. Young-Fadok, K. HallLong, E.J. McConnell, G. Gomez Rey, R.L. Cabanela,
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Original Research
Laparoscopic resection for primary and recurrent Crohn's disease: A case series of over 100 consecutive cases Sofoklis Panteleimonitis a, b, *, Jamil Ahmed a, Thomas Parker a, Tahseen Qureshi a, c, Amjad Parvaiz a, b, d a
Poole Hospital NHS Trust, Longfleet Road, Poole, United Kingdom University of Portsmouth, School of Health Sciences and Social Work, Portsmouth, United Kingdom Bournemouth University School of Health and Social Care, Bournemouth, United Kingdom d Champalimaud Foundation, Lisbon, Portugal b c
h i g h l i g h t s Laparoscopic resection surgery for Crohn's disease is safe and feasible. In the hands of experienced laparoscopic surgeons conversion rates are minimal (4.7% in our series). Laparoscopic surgery is a viable option for patients having recurrent or emergency resection surgery for Crohn's disease.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 May 2017 Received in revised form 13 September 2017 Accepted 16 September 2017 Available online 22 September 2017
Background: Laparoscopic surgery for patients with Crohn's disease (CD) is considered challenging. The aim of this study is to evaluate the clinical outcomes of laparoscopic bowel resection in patients with CD. We also assessed the effectiveness of the laparoscopic approach in recurrent or emergency surgery due to CD. Materials and methods: All patients with CD, who underwent laparoscopic resection surgery in two units from October 2006 to February 2016, were identified through prospectively maintained databases. Their baseline characteristics and perioperative outcomes were analysed. The outcomes of patients receiving primary vs recurrent and elective vs emergency laparoscopic resections for CD were also examined. Results: In total 106 patients underwent laparoscopic resection. Primary ileocolic resection was the most frequent procedure (62%) followed by redo-ileocolic resection (15%). Overall conversion rate was 4.7%, median operative time was 130 (95e185) minutes and length of stay was 4 days (3e6). There was one anastomotic leak (1.1%) and 30-day re-operation rate was 5.7%. Patients having primary resections were younger and had a shorter length of stay (4 vs 5 days; p ¼ 0.014). Thirty day re-operation rate was higher in patients having emergency surgery (3.1% vs 30%; p ¼ 0.011). Conclusions: This case series demonstrates that laparoscopic resection surgery for CD is safe and feasible. Similarly, laparoscopic surgery is also a viable option for patients having recurrent resection and possibly even emergency surgery. Crown Copyright © 2017 Published by Elsevier Ltd on behalf of IJS Publishing Group Ltd. All rights reserved.
Keywords: Crohn's disease Laparoscopy Colorectal surgery
1. Introduction Despite advances in the medical management of Crohn's disease
* Corresponding author. University of Portsmouth, School of Health Sciences and Social Work, James Watson West, 2 King Richard 1st Road, Portsmouth, PO1 2FR, United Kingdom. E-mail address: [email protected] (S. Panteleimonitis).
(CD) the majority of Crohn's patients will undergo surgical treatment during their lifetime [1e6]. In addition, 40e50% of patients that receive surgical treatment for Crohn's will require further surgery within the next 10e15 years [6e10]. Laparoscopy has become the gold standard throughout the developed world for the majority of gastrointestinal procedures [10,11]. However, Crohn's patients are often considered poor candidates for laparoscopic surgery due to the nature of the disease. It often involves extensive
https://doi.org/10.1016/j.ijsu.2017.09.055 1743-9191/Crown Copyright © 2017 Published by Elsevier Ltd on behalf of IJS Publishing Group Ltd. All rights reserved.
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inflammation, thickened mesentery, skip lesions throughout the bowel and enteric fistulae [12]. Despite the challenges of laparoscopic surgery in patients with CD, Crohn's patients have potentially a lot to gain from this approach. Considering their young age and frequent need for repeated operations the benefits of improved cosmesis, less postoperative pain, shorter length of stay, earlier return to work, reduced adhesional formation and reduced incidence of incisional hernias due to the conservation of abdominal wall integrity are undeniably appealing [1,13,14]. These benefits have led to many laparoscopic surgeons to adopt a minimally invasive approach for patients with CD over the last two decades and it is now feasible to perform the whole range of CD interventions laparoscopically [2]. There are a number of case series describing laparoscopy in patients with CD [12,15e17]. Studies have also shown that the laparoscopic approach has better short and long-term outcomes when compared to open surgery [1,18e22]. The objectives of this study are to investigate the safety and feasibility of laparoscopic bowel resection for CD and assess its feasibility for recurrent and emergency CD surgery. To achieve this we describe the peri-operative and short term outcomes of patients receiving laparoscopic resection surgery for CD from two centres in the United Kingdom over the last 9 years. We also compare the outcomes of primary laparoscopic resections with redo laparoscopic resections for recurrent disease and the outcomes of laparoscopic resections in an elective vs emergency setting. To our knowledge, this is the largest series of laparoscopic bowel resections for CD in the UK to date. 2. Materials and methods All patients with CD, who underwent laparoscopic surgery in two National Health Service (NHS) units in the UK from October 2006 to February 2016, were identified through prospectively maintained databases. Patients undergoing primary, redo, elective and emergency laparoscopic resections were included in the analysis. Inclusion criteria were: all patients receiving laparoscopic bowel resection surgery for CD. Exclusion criteria were: non-bowel resection surgery (e.g. stricturoplasty), open surgery and surgery for ulcerative colitis or cancer. Two experienced laparoscopic colorectal surgeons performed or closely supervised all procedures in each unit. Both surgeons had vast experience in laparoscopic colorectal benign and malignant surgery and both surgeons were trainers for the LAPCO training programme, the UK's national training programme for laparoscopic colorectal surgery [23]. Surgeon A was the senior surgeon who trained surgeon B, hence both surgeons applied the same standardised modular approach to surgery [24] and peri-operative care regime. Informed consent was obtained from all patients. Appropriate approval for the study was obtained by Poole Hospital NHS Trust. The study was registered with ResearchRegitry.com (Unique Identification Number: researchregistry2518) and the research work has been reported in line with the PROCESS criteria [25]. Data was collected prospectively and analysed for baseline characteristics, peri-operative data and short term post-operative data. Conversion was defined as any incision needed to either mobilise the specimen or ligate the vessels. For a procedure to be considered laparoscopically completed there should be no conversion as defined above. Converted patients were included in the analysis as we performed an intention to treat analysis. 2.1. Peri-operative care Pre-operative workup included computer tomography (CT) and or magnetic resonance imaging (MRI) enteroclysis, ultrasound
examinations and colonoscopy to exclude or assess colonic disease. Laparoscopy was the default approach for all patients with surgeries either performed or closely supervised by the consultant surgeons, with the consultant surgeon always scrubbed for all cases. The only contra-indication to laparoscopy was patients not deemed anaesthetically fit to tolerate pneumoperitoneum. However, one should note that these patients are rarely fit for open surgery either. Patients with complex problems were discussed at the inflammatory bowel disease multidisciplinary team meeting (IBD MDT) and referred for resection if deemed necessary. Indications for surgery included: failure of medical management, fistulating disease, obstructing stricture and abdominal sepsis due to perforation, abscess or mass. Post-operative care was standardised, with patients entering a routine enhanced recovery programme and receiving follow up from a multi-disciplinary team of health care professionals including the colorectal team, the gastroenterologists, the nutrition team and the stoma nurses. Antibiotics were only given routinely on induction, where a single intravenous dose of 1.5gr cefuroxime and 500 mg metronidazole was given. A single shot spinal infiltration containing a mixture of diamorphine and marcaine was given prior to anaesthesia for analgesia, no epidural catheters were used and wounds were infiltrated with local anaesthetic. After surgery patients were encouraged to drink fluids on the same evening, get out of bed as soon as possible and eat solids as soon they felt to and once oral fluids were tolerated. Intravenous hydration was removed as soon as the patient could tolerate oral fluids, urinary catheters were taken out the morning after surgery and analgesia was carried out with oral paracetamol and ibuprofen. All patients undergoing emergency or urgent resections were on immunosuppressive medication and could not be taken off this medication prior to surgery. Patients receiving elective surgery had their immunosuppressive medication tapered off and stopped four weeks prior to surgery. All patients having emergency resections had poor nutritional statuses while elective patients were nutritionally optimised and had a normal nutritional status; defined as a serum albumin level that was over 30 gr/liter.
2.2. Operative technique All procedures were performed through a well-established standardised modular technique [24]. This approach permits a safe and reproducible technique that also facilitates teaching and training [24]. Since most of the procedures performed were ileocolic resections, we describe its operative technique as below. The patient was placed in the modified Lloyd Davies position. The optical port was placed infra umbilical in the midline with the open Hassan technique and pneumoperitoneum was established. In case of a previous midline scar, open technique for insufflation was performed in the left upper abdomen. Pressure was set to 12 mmHg. Further ports were inserted under direct vision and placement is described in Fig. 1. For the initial setting the patient was placed in the reversed Trendelenburg position with the left sided tilted down. The omentum was retracted cranially over the upper compartment and the transverse colon was exposed. The small bowel was moved to the left side to expose the duodenal area. Surgical dissection is divided into the following steps: 1 2 3 4
Vessel Control with medial to lateral dissection Sub-ileal dissection Lateral Mobilization Hepatic Flexure Mobilization (if required)
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Table 1 Baseline characteristics of patients with Crohn's disease. Total (n ¼ 106) Sex Male Female Median age (IQRa) Mean BMI (SDb) ASA grade I II III IV Surgeon A B Urgency Elective Emergency a b
48 (45.3%) 58 (54.7%) 40 (29e52.25) 23.8 (4.16) 12 75 13 1 65 41 96 (90.6%) 10 (9.4%)
IQR: Inter-quartile range. SD: standard deviation.
previous abdominal surgery. Of those 19 had received previous resectional surgery for CD, including 18 ileocolic resections and one anterior resection. The remaining patients having previous abdominal surgery included four appendicectomies, one laparotomy, three ileostomies, two hysterectomies and a Caesarean. All previous abdominal surgeries were open procedures. 3.2. Operative outcomes Fig. 1. Port placement for ileocolic resection.
5 Specimen extraction and extracorporeal side-to-side stapled/ mechanical anastomosis using a TLC75 ETHICON PROXIMATE® Linear Cutter stapler During early experience a 10 mm LigaSure Atlas™ Covidien energy device was used to seal the thick mesentery. Subsequently, when the 5 mm LigaSure device became available we routinely performed procedures using this energy source to seal and divide the mesentry. Vessels were isolated and ligated with haem-olocks™. Vessel control was always done laparoscopically. The usual extraction site was in the midline at the peri-umbilical port site. A transverse incision in the right side of the abdomen was avoided as it could be used for future stoma formation. At the end of the procedure a check laparoscopy was performed to look for haemostasis. Drains and nasogastric tubes were avoided. 2.3. Statistics methods IBM SPSS version 22 (SPSS Inc., Chicago, IL, USA) and Microsoft Excel 2010™ were used for the statistical analysis. Data was expressed as median with interquartile range for non-parametric data and mean with standard deviation for parametric data. Clinical characteristics were compared using c2 test or Fishers exact test for categorical variables and Mann-Whitney U test (nonparametric) and t-test (parametric) for continuous variables. 3. Results 3.1. Demographics One hundred and six patients underwent laparoscopic surgery for CD between October 2006 and February 2016. Their baseline characteristics are shown in Table 1. Thirty (28.3%) patients had
Primary ilieocolic resection was the most frequent procedure, 62.3% (n ¼ 66), followed by redo-ileocolic resection, 15.1% (n ¼ 16). There were 3 small bowel resections, with the remaining procedures being colonic resections: 7 panproctocolectomies, 6 subtotal colectomies, 4 proctocolectomies, 2 sigmoid colectomies, 1 abdominoperineal resection and 1 right and sigmoid colectomy. Fig. 2 provides a patient flowchart of the procedures performed, dividing them in primary vs recurrent, emergency vs elective and stating which procedures required re-operations. Five procedures were converted to open (4.7% conversion rate). Median operative time was 130 min (95e185) and median blood loss 20 mls (0e50). The operative outcomes are summarised on Table 2. 3.3. Post-operative outcomes The details of post-operative outcomes are illustrated in Table 2. Median length of stay was 4 days (3e6). Thirty day re-operation rate was 5.7% (n ¼ 6). Regarding those, five of them were following primary ileocolic resections and half of them (n ¼ 3) were following emergency surgery. One of them was done for an anastomotic leak, two were done secondary to small bowel obstruction, two were done for suspected sepsis with subsequent normal intraoperative findings and one was an evacuation of a haematoma. There were 18 (17%) 30-day readmissions; these were due to a variety of reasons including 5 patients readmitted with nausea and vomiting, 4 with non-specific abdominal pain, 2 with a wound infection, a patient with an infected haematoma that was treated with antibiotics, a patient with a subhepatic collection that was treated conservatively, a patient admitted with acute kidney injury and small bowel obstruction that settled with conservative measures, a patient with ileus and haematoma that developed a subsequent pulmonary embolus during readmission, two patients with small bowel obstruction and one with an anastomotic leak. The latter 4 patients required surgery during their readmission and are
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Fig. 2. Patient flowchart.
Table 2 Peri-operative and short term post-operative outcomes of patients with Crohn's disease. Total (n ¼ 106) Conversion to open Median operative time in minutes (IQRa) Median blood loss in mls (IQR) Median length of stay in days (IQR) 30-day readmissions 30-day re-operations Anastomotic leaks 30-day mortality a
5 (4.7%) 130 (95e185) 20 (0e50) 4 (3e6) 18 (17.0%) 6 (5.7%) 1 (1.1%) 0
IQR: Inter-quartile range.
included in the 30-day re-operation group (Clavien-Dindo 3b). The
remaining of the readmissions were grade 1e2 in the ClavienDindo scale. Regarding the patient with the anastomotic leak, he presented on day 6 post-op with a right upper quadrant abscess (collection). It is difficult to pin point the exact cause of the leak although there was no obvious bowel ischaemia.
3.4. Primary vs recurrent resections The outcomes of patients undergoing primary resections vs redo resections for CD are presented in Table 3. The primary group consisted of 66 ileocolic resections, two small bowel resections and 19 colonic resections while the recurrent group consisted of 16 redo-ileocolic resections, one small bowel resection and 2 colonic resections.
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Table 3 Baseline characteristics and surgical outcomes of primary vs recurrent resections for Crohn's disease.
Median age (IQRa) Mean BMI (SDb) Conversion rate Median operation time (min) Median blood loss (mls) Median length of stay (days) 30-day readmission rate 30-day re-operation rate Anastomotic leak rate
Primary resection (n ¼ 87)
Recurrent (n ¼ 19)
P value
36 (28e49) 23.6 (4.01) 4 (4.6%) 127.5 (90e183.75) 20 (0e50) 4 (3e6) 13 (14.9%) 6 (6.9%) 1 (1.4%)
48 (42e68) 25 (4.83) 1 (5.3%) 145 (123.75e185.75) 20 (10e50) 5 (4.25e7.75) 5 (26.3%) 0 0
0.001m 0.228t 1.000f 0.147m 0.661m 0.014m 0.309f 0.589f 1.000f
m: Mann-Whitney U. t: t-test. f: Fischer's exact test. a IQR: Inter-quartile range. b SD: standard deviation.
There was no difference in the conversion rate between patients having primary or recurrent surgery for CD (4.6% vs 5.3%; p ¼ 1.000). None of the converted patients having primary surgery for CD had any other form of previous abdominal surgery. Patients having primary resections tended to be younger than those having recurrent resection surgery (p ¼ 0.001). Apart from length of stay, which was one day longer in patients undergoing recurrent resections (4 vs 5 days; p ¼ 0.014), there was no statistical difference in any of the other short-term surgical outcomes. 3.5. Elective vs emergency resections The outcomes of patients undergoing elective and emergency laparoscopic resection surgery for CD are summarized is Table 4. The elective group consisted of 58 ileocolic resections, 16 redoileocolic resections, 3 small bowel resections and 19 colonic resections while the emergency group consisted of 8 ileocolic resections and 2 colonic resections. Thirty day re-operation rate was higher in patients having emergency surgery (3.1% vs 30%; p ¼ 0.011). Length of stay appeared to be longer in the emergency group but this did not reach statistical significance (4 vs 8 days, p ¼ 0.115). There were no statistically significant differences in any of the other outcomes between the two groups. 4. Discussion This study shows that laparoscopic surgery is feasible with a low conversion rate, acceptable operative time, minimal blood loss and
good post-operative outcomes. Furthermore, this case series also demonstrates that disease recurrence and an emergency setting (in haemodynamically stable patients) are not contraindications for laparoscopic surgery. The majority of patients requiring resection surgery for CD underwent ileocolic resections. This is in accordance with the prevalence of the disease, which tends to predominantly affect the terminal ileum [10,12]. The conversion rate was 4.7%, which includes all patients undergoing resection surgery for CD. This is despite 28.3% of patients induced in this study having received previous open abdominal surgery. Our conversion rate supports the feasibility of laparoscopic surgery in CD and is in accordance with the published evidence, in which conversion rate varies between 2% and 42% for patients with CD [12,20,22,26,27]. The variation found in the literature is probably due to differences in defining a conversion to open, variability in laparoscopic experience among the operating surgeons, disease severity and site of affected segment [26,28e30]. It is worth noting that a recent study by Masoomi et al. examining the American National Inpatient Sample (NIS) database reported a conversion rate for patient's receiving laparoscopic surgery for CD of 20% and concluded that Crohn's is a strong predictor for conversion in laparoscopic surgery [31]. This is in contrast to our findings and those of other published reports [1,2,12,22,32], where conversion rates were comparable to that of laparoscopic colorectal oncological surgery. The most likely explanation for this difference is the variability of laparoscopic experience of the performing surgeons. The NIS database includes a huge cohort of surgeons with variable laparoscopic experience. In contrast, the conversion rate reported by Nguyen et al. [12] in 335
Table 4 Baseline characteristics and surgical outcomes of elective vs emergency surgery for Crohn's disease.
Median age (IQRa) Mean BMI (SDb) Conversion rate Median operation time (min) Median blood loss (mls) Median length of stay (days) 30-day readmission rate 30-day re-operation rate Anastomotic leak rate m: Mann-Whitney U. t: t-test. f: Fischer's exact test. Bold value signifies p < 0.05. a IQR: Inter-quartile range. b SD: standard deviation.
Elective resections (n ¼ 96)
Emergency (n ¼ 10)
P value
40.5 (30.25e52.75) 24 (4.19) 4 (4.2%) 130 (95e182.5) 20 (0e50) 4 (3e6) 16 (16.7%) 3 (3.1%) 1 (1.3%)
35 (23.5e53.75) 21.6 (3.26) 1 (10%) 120 (92.5e200) 20 (0e35) 8 (3e18.5) 2 (20%) 3 (30%) 0
0.479m 0.139t 0.397f 0.953m 0.506m 0.115m 0.677f 0.011f 1.000f
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cases of laparoscopic resections for CD is only 2%. In this study the procedures were performed by surgeons with vast laparoscopic experience in a tertiary centre for CD. Equally, in our cohort all procedures were performed by experienced laparoscopic surgeons, which accounts for our low conversion rate. Median operative time in our study was 130 min for all resections, 127.5 min in primary resections and 145 min in patients with recurrent disease. Operative time is variable across the literature, ranging between 85 and 185 min for first ileocolic resection [7,15,16,20,32,33] and 118e215 min for recurrent ileocolic resections [15,16,29,34]. In our study, operative time appeared shorter in patients receiving primary resections compared to those with recurrent disease (Table 3), but this did not reach statistical significance. Previous studies have reported contradictory results, with some demonstrating shorter operative times in primary laparoscopic Crohn's resections when compared to recurrent resections [7,16], with other studies reporting no difference [15,35]. The post-operative outcomes of this study reinforce the acumen that laparoscopic surgery is safe and feasible in the hands of surgeons with appropriate laparoscopic experience. The median length of stay was 4 days, while in previous studies the length of stay tends to range between 5 and 7 days in primary resections [18e20,32,36] and up to 9 days in recurrent ones [2,15,16,29,34]. Thirty day readmission rate, reoperation rate and overall anastomotic leak rate were acceptable in our cohort (Table 2), further demonstrating the feasibility of the laparoscopic approach for this type of surgery. Previous evidence comparing anastomotic leak rate and morbidity of open vs laparoscopic Crohn's surgery after first ileocolic resection supports this, with studies showing similar outcomes [10,20,22,33] or outcomes favouring the laparoscopic approach [18,19]. It is important to note that all patients entered an enhanced recovery after surgery programme (ERAS), which has a major role in the post-operative outcomes presented. It is hard to know in what degree the post-operative outcomes presented are due to laparoscopy or the ERAS programme. The majority of our patients that were readmitted were due to Clavien-Dindo grade 1e2 complications, with only 4 (22%) being readmitted with grade 3 complications or above. The commonest causes were non-specific abdominal pain and nausea and vomiting. Even though no formal diagnosis was given for these patients they all settled with conservative measures (Clavien-Dido grade 1). Comparison of the outcomes of patients having laparoscopic surgery for primary vs recurrent resections showed that patients having primary resections tend to be younger and have a shorter length of stay (Table 3). Patients requiring recurrent resection surgery tend to be older since they have already had their primary surgery earlier in their lives. Patients requiring recurrent resection surgery for Crohn's can be sicker and their surgery is often more technically demanding. This might explain why patients in the recurrent cohort stayed in hospital an extra day. Nevertheless, this was not reflected in any of the other peri- and post-operative outcomes and although median operation time and 30-day readmission rate were also higher in the recurrent cohort, they were not statistically significant (Table 3). These results are in accordance with previously published reports that have shown similar postoperative outcomes for patients receiving surgery for primary vs recurrent disease [15,16]. Furthermore, conversion rate was similar between the two groups. One might have expected to find a higher conversion rate in surgery for recurrent disease, due to the formation of adhesions. However, the majority of the evidence dismisses that [7,15,16] as does our study (Table 3). Patients having emergency surgery for CD had a higher 30-day re-operation rate (Table 4). This is probably a reflection of the poor physiological state of these patients, which are usually acutely unwell and have been on high dose of immunosuppressive agents.
This is contrast to patients receiving elective surgery who have been tapered off their immunosuppressive medication and are in a nutritionally acceptable status. This can explain why patients in the emergency cohort stayed in hospital twice as long (4 vs 8 days), although this did not reach statistical significance due to the small number of cases in the emergency group (n ¼ 10). It should be noted that although the re-operation rate was higher in the emergency group, there were only three re-operations. One of them was an evacuation of a haematoma and two were laparoscopies, one of which was negative (see Fig. 2). Considering the small number of emergency patients in this study these results need to be taken into account with caution. Moreover, in this series all patients operated on an emergency setting were haemodynamically stable and only patients deemed by the anaesthetist as fit enough to tolerate a pneumoperitoneum received laparoscopic surgery. Therefore, the conclusions derived regarding emergency patients in this study only apply for stable patients. So far the published evidence for emergency laparoscopic surgery for CD is mainly limited to case reports as its application is still on debate [37,38]. However, since laparoscopy for abdominal surgical emergencies is gaining increasing acceptance it is likely that laparoscopic emergency surgery for CD will become more common. In this study three patients were operated on because of fistulating disease and two because of intra-abdominal abscesses. It is worth noting that despite the pathology of these patients, they were all operated on in an elective setting, none of them had an anastomotic leak and none of them were readmitted or re-operated on within 30 days. We acknowledge the limitations of this study, being retrospective in nature and essentially a description of a case series. In addition, we have not reported minor post-operative complications (Clavien-Dindo 1e2). This is because on our data set we only record complications that result in re-operation, re-intervention (ClavienDindo grade 3 or more) or complications resulting in a readmission. It is conceivable that minor complications (Clavien-Dindo 1e2) would be reflected in prolonged hospital stay which was not the case for our study. Another limitation might be that the experience of the two surgeons might not be reflective of the much wider cohort of surgeons performing laparoscopic colorectal surgery. Regardless, considering our large sample size and study design, we believe our study has enough power to demonstrate the feasibility of laparoscopic Crohn's surgery in the hands of experienced laparoscopic surgeons where operative technique and post-operative treatment have been standardised. Furthermore, the majority of the current evidence in this topic is based on non-randomised, retrospective studies with small sample size numbers. Findings throughout the literature seem to consistently support the feasibility of laparoscopy for CD. Even though larger scale randomised control trials comparing laparoscopic vs open surgery would be desirable in order to obtain concrete evidence [3], considering the amount of current evidence one could debate that performing such a study on this group of relatively young and slim patients might be against the patients best interests. 5. Conclusions In summary, this study has shown that laparoscopic resection surgery for CD is safe and feasible when operative technique and post-operative care has been standardised in the hands of experienced laparoscopic colorectal surgeons. Furthermore, this study demonstrated that laparoscopic surgery is a viable option for patients with recurrent disease and possibly even those undergoing emergency surgery, if haemodynamically stable. Considering the majority of the previous studies examining the feasibility of laparoscopic surgery for CD have small sample sizes
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this study enriches the available literature since it presents the largest case series in the UK so far. In addition, it is unique since it compares the outcomes of both primary vs recurrent and elective vs emergency laparoscopic CD resection surgery. Further larger scale multicentre case series are needed to solidify the feasibility and safety of laparoscopy for CD. Ethical approval Ethical approval was not required since the study is a retrospective case series with no patient identifiable data. According to the Health Research Authority (HRA), this study was not classified to need their approval. The study was approved by Poole Hospital NHS Trust. Funding No funding was obtained in order to perform or write up this study. Author contribution Conception and design: Sofoklis Panteleimonitis, Amjad Parvaiz. Analysis and interpretation of the data: Sofoklis Panteleimonitis, Thomas Parker. Drafting of the article: Sofoklis Panteleimonitis. Critical revision of the article for important intellectual content: Jamil Ahmed, Amjad Parvaiz, Tahseen Qureshi. Final approval of the article: Amjad Parvaiz, Tahseen Qureshi. Conflict of interest No conflicts of interest to declare by any of the authors. Research Registration Unique Identifying Number (UIN) The study was registered with ResearchRegistry.com. The Unique Identification Number is researchregistry2518. Guarantor Sofoklis Panteleimonitis. Professor Amjad Parvaiz. Acknowledgement We thank Karen Flashman for her hard work on maintaining the surgical database on daily basis. References [1] J.Y. Lim, J. Kim, S.Q. Nguyen, Laparoscopic surgery in the management of Crohn's disease, World J. Gastrointest. Pathophysiol. 5 (2014) 200e204, https://doi.org/10.4291/wjgp.v5.i3.200. [2] M. Tavernier, G. Lebreton, a Alves, Laparoscopic surgery for complex Crohn's disease, J. Visc. Surg. 150 (2013) 389e393, https://doi.org/10.1016/ j.jviscsurg.2013.09.004. [3] S. V Patel, S.V.B. Patel, S. V Ramagopalan, M.C. Ott, Laparoscopic surgery for Crohn's disease: a meta-analysis of perioperative complications and long term outcomes compared with open surgery, BMC Surg. 13 (2013) 14, https:// doi.org/10.1186/1471-2482-13-14. [4] R.D. Cohen, J.F. Tsang, S.B. Hanauer, Infliximab in Crohn's disease: first anniversary clinical experience, Am. J. Gastroenterol. 95 (2000) 3469e3477, https://doi.org/10.1111/j.1572-0241.2000.03363.x. [5] V. Binder, H. Both, P.K. Hansen, C. Hendriksen, S. Kreiner, K. Torp-Pedersen, Incidence and prevalence of ulcerative colitis and Crohn's disease in the County of Copenhagen, 1962 to 1978, Gastroenterology 83 (1982) 563e568. [6] O. Bernell, A. Lapidus, G. Hellers, Risk factors for surgery and recurrence in 907 patients with primary ileocaecal Crohn's disease, Br. J. Surg. 87 (2000)
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