Endoscopic and Clinical Recurrences After Laparoscopic or Open Ileocolic Resection in Crohn's Disease

Abstract

Background:

After ileocolic resection in Crohn's disease, studies concerning the influence of the laparoscopic or open approach on clinical and endoscopic recurrences are scarce.

Patients and Methods:

In a prospective database, we identified all patients operated on between 2004 and 2012 for primary ileocolic resection in Crohn's disease, with at least 6 months of follow-up. The rates of endoscopic recurrence during the first postoperative year and the clinical recurrence at any time during follow-up were measured and compared after the laparoscopic or open approach.

Results:

Sixty-two patients (mean±standard deviation age, 33.5±12.7 years; 35 females) were operated on through laparoscopy (n=28) or laparotomy (n=34). Medical treatment, evolution and phenotype of disease, and postoperative course were comparable in both groups. Mean±standard deviation follow-up was 3.5±1.9 years. Ileocolonoscopy was available in 46 (74.2%) patients. Normal endoscopy or minor recurrence (i0 or i1 grade) was significantly more frequent after laparoscopy (14/24 [58.3%]) versus laparotomy (5/22 [22.7%]) (P=.019). Clinical recurrence was comparable at 1 year (P=.116) and at the end of follow-up (P=.799) after laparoscopy (28.6% and 50%, respectively) or laparotomy (11.8% and 55.9%, respectively).

Conclusions:

After resection, normal or minor endoscopic lesions (i0 or i1 grade) were more frequent after laparoscopy than after laparotomy. However, clinical recurrence was similar after both techniques.

Introduction

Despite advances in medical treatment during the last two decades, such as immunosuppressants (IS) or anti-tumor necrosis factor-α (TNFα), surgery is still an important therapeutic option in patients with luminal Crohn's disease (CD). Even in recent studies, at the era of these new treatments, 25% of patients still require abdominal surgery in the first 5 years after CD diagnosis.¹ Distal ileal or ileocolic locations are most common in luminal CD, and ileocolic resection is the most frequently performed surgical procedure for treatment of CD: up to 75% of patients requiring abdominal surgery for their luminal CD will have ileal or ileocolic resection.² Disease recurrence concerns the vast majority of the patients, and endoscopic recurrence is known to precede clinical relapse: at 1 year endoscopic recurrence rates range from 48% to 93%, and clinical recurrence has been demonstrated in 10%–38% of patients.^3,4

Laparoscopy has gained wide acceptance in gastrointestinal surgery, with demonstrated faster return to normal diet and activity, reduced hospital stay, reduced postoperative pain, and better cosmesis,⁵ and its use is accepted in benign and malignant colorectal diseases.^6,7 Laparoscopic surgery offers additional advantage of smaller abdominal fascial wounds, low incidence of hernias, and decreased rate of adhesive small bowel obstruction compared with conventional surgery, reducing the need for non–disease-related surgical procedures in the CD population. Moreover, the laparoscopic approach has been suspected to minimize the immune response, with possible impact on cancer behavior and nonmalignant diseases.^8,9 Many studies have compared laparoscopic with open ileocolic resection for feasibility and postoperative course, demonstrating that laparoscopic ileocolic resection for CD, even for complex procedures,¹⁰ is feasible and safe.^11–13 Nevertheless very few of them have reported the clinical and endoscopic evolution after surgery.^14,15

The aim of this study was to evaluate and compare the clinical and endoscopic progression of patients with CD at short- and mid-term intervals, following laparoscopic ileocolic resection compared with conventional surgery, in the era of IS and anti-TNFα.

Patients and Methods

Patients

Records of patients who underwent an elective ileocolic resection for CD at our tertiary referral teaching hospital, between February 2004 and January 2012, were identified from a prospectively designed and maintained database. After institutional review board approval, this database was retrospectively reviewed to identify patients with diagnosis of ileal or ileocolic CD (L1 location in the Montreal classification¹⁶) scheduled for an elective ileocolic resection, without any previous bowel resection, and completing at least 6 months of follow-up. All patients had ileocolonoscopy with biopsies to establish the diagnosis, as well as small bowel computed tomography and/or magnetic resonance imaging to assess extent and activity of CD. When suspected, a computed tomography scan was performed to identify and treat abscesses.

Following preoperative, intraoperative and postoperative data were collected: patient's general condition and comorbidities, time elapsed since the diagnosis of CD, phenotype and complications of CD, treatments (medical, surgical, and radiological) before the intervention, open or laparoscopic surgery and operative findings, type of postoperative complications according to the Clavien–Dindo classification,¹⁷ pathological findings, clinical evaluation at 1 year and at the end of the follow-up, and the endoscopic results during the first postoperative year according to the classification of Rutgeerts et al.¹⁸ Endoscopic recurrence was defined by inflammation or ulceration on the neo-terminal ileum or the anastomosis and was considered significant when the Rutgeerts score was ≥i2; clinical recurrence was defined by any abdominal symptom of CD, confirmed by biological assessment or imaging, excluding anal or extradigestive symptoms.

Operative procedures

Patients were operated on either by a laparoscopic (LAP group) approach or by a laparotomy (OPEN group). All procedures were done by or supervised by colorectal and/or laparoscopic senior surgeons. The choice of operative technique was the decision of the operating surgeon.

All procedures were performed with the patient under general anesthesia with orotracheal intubation. For laparoscopy (LAP group), patients were operated on using one or two 5-mm trocars (suprapubic and/or right lower quadrant) and two 10-mm trocars (umbilical and left lower quadrant). After ileocolic mobilization, this umbilical port-site incision was enlarged to a 3.5–5-cm umbilical midline incision for exteriorization and resection of the diseased segment and complete small bowel exploration. Intestinal continuity was restored either by side-to-side or end-to-side ileocolic anastomosis using either a double-stapled technique or by hand-sewn ileocolic anastomosis. Associated small bowel resection included resection of intestinal segments involved in enteroenteral fistulas or resection of proximally located small bowel strictures located in a segment other than ileocecal. Associated colon resection included resection of distant colonic segments involved in enterocolic fistulas. Synchronous surgery of the small bowel or colon was performed through the same short umbilical incision. Conversion to an open surgery was defined as any unplanned incision or a planned incision longer than 6 cm. All Open group cases were performed via a lower midline laparotomy with the umbilicus as its upper limit. The small bowel was explored, and intestinal continuity was restored according to the same technique used in the LAP group.

Postoperative care included progressive oral feeding starting on postoperative day 1, early mobilization, and prevention of deep venous thrombosis by low-molecular-weight heparin and stockings and, when required, by drainage removal from postoperative day 2.

Follow-up

Follow-up consisted in clinical examination by the operating surgeon at 1 month after intervention and by a senior gastroenterologist specializing in inflammatory bowel disease at postoperative months 6, 12, and 24 and at any time when required by patients. According to the ECCO guidelines,¹⁹ postoperative ileocolonoscopy was scheduled between postoperative months 6 and 12 and was performed by the same gastroenterologist; it explored the entire rectocolon, the anastomosis, and the neo-terminal ileum on its last 20–30 cm.

Study end points

The main end point was the recurrence of CD, considered on the endoscopic examination during the first postoperative year, and clinical symptoms at any time during follow-up. Secondary end points were complication rates in both groups.

Statistical analysis

Comparisons between the two groups were analyzed by Fisher's exact test, the Mann–Whitney U test, or Student's t test for quantitative and qualitative variables, when appropriate. Significance was defined as P<.05.

Results

Preoperative data, surgical intervention, and postoperative course

During the study period, 101 patients underwent elective ileocolic resection for CD. Eighteen patients had a history of previous bowel resection, and 21 had less than 6 months of follow-up; they were excluded from our study. Thus, 62 patients met our criteria for analysis and were the population of this study. Among the 62 patients, there were 35 women (56.45%). Mean±standard deviation age was 33.48±12.7 years (range, 17.1–59 years), and mean±standard deviation duration of CD prior to surgery was 7.09±8.10 years (range, 0.19–36 years). Medical treatment during the history of CD included aminosalicylates, steroids, IS, and anti-TNFα in 39 (62.90%), 43 (69.35%), 33 (53.23%), and 10 (21.6%) patients, respectively. During the 3 months preceding surgery, medical treatment included aminosalicylates, steroids, IS, and anti-TNFα in 9 (14.52%), 9 (14.52%), 19 (30.64%), and 6 (9.68%) patients, respectively. Three patients (4.84%) had been operated on for surgical drainage of an intraabdominal abscess.

Thirty-four patients were operated on through conventional laparotomy (54.84% [Open group]) and 28 through laparoscopy (45.16% [LAP group]). Recourse to laparoscopy was significantly more important at the end of the study (13 laparoscopies in 15 patients during the last 2 years versus 4 laparoscopies in 18 patients during the first 2 years; P=.0003). In the LAP group, conversion to an open procedure was required in 9 patients (32.14%), for intense inflammatory lesions in the right lower quadrant and/or unplanned associated bowel resection (n=7) or for obesity (n=1) and small bowel adhesions (n=1).

Characteristics of patients and operative data were similar in both groups. Medical treatments during the history of CD or during the 3 months preceding surgery were comparable in both groups (Table 1).

Table 1.

Characteristics of 62 Patients Operated on for Ileocolic Resection in Crohn's Disease

	LAP (n=28)	Open (n=34)	P
Age (years)	31.69±13.33	34.96±12.16	.32
Sex (M/F)	10/18	17/17	.31
Active tobacco consumption	6	10	.566
BMI (mean±SD) (kg/m²)	22.43±10.86	22.11±3.41	.794
Mean±SD duration of CD prior to surgery (years)	5.28±6.09	8.58±9.27	.098
Previous treatment during the history of CD
Aminosalicylates	16	23	.437
Steroids	18	25	.581
Immunosuppressant	16	17	.617
Anti-TNFα	7	3	.163
Treatment during the 3 months before surgery
Aminosalicylates	6	3	.277
Steroids	3	6	.494
Immunosuppressant	9	10	1
Anti-TNFα	5	1	.082
Perianal disease	5	10	.377
Penetrating behavior	12	16	.801
Preoperative abcess	5	11	.249
Fistula	8	13	.590
Stricturing behavior	22	24	.566
Double-stapled anastomosis	12	10	.298
Side-to-side anastomosis	24	23	.139
Associated small bowel resection	3	5	.719
Associated colon resection	2	3	1
Mean±SD length of resected small bowel (cm)	32.9±22.8	36.4±18.5	.527
Temporary stoma	2	8	.097
Microscopically involved resection margin	3	10	.116
Uneventful postoperative course	24	27	.739
Median (range) hospital stay (days)	7 (5–20)	8 (6–30)	.004^a
Preventive medical treatment within the first year	15	21	.608

Significant difference.

BMI, body mass index; CD, Crohn's disease; F, female; LAP, laparoscopic group; M, male; SD, standard deviation; TNFα, tumor necrosis factor-α.

Postoperative course was uneventful in 24 (85.71%) and 27 (79.41%) patients in the LAP and Open groups, respectively (P=.739). Severity of complications according to the Clavien–Dindo score was comparable in both groups: grade 2 for 1 patient in each group (one prolonged ileus and one colitis) and grade 3 for 3 patients in LAP group (three intraabdominal abcesses) versus 4 patients in the Open group (two intraabdominal abcesses and two findings of postoperative peritonitis). Ten (LAP group [n=2] and OPEN group [n=8]; P=.097) patients required temporary stoma (16.13%): 8 during the ileocolic resection and 2 following anastomotic leakage. There were no deaths in either group. Median postoperative stay was significantly shorter in the LAP group (7 days; range, 5–20 days) than in the Open group (8 days; range, 6–30 days) (P=.004).

Endoscopic and clinical follow-up

Mean postoperative follow-up was 3.53±1.96 years. Complete ileocolonoscopy was performed in 46 (74.19%) patients: 24 of 28 (85.71%) in the LAP group and 22 of 34 (64.71%) in the Open group), after a mean delay of 0.6±0.2 years. Severity of postoperative endoscopic recurrence according to the Rutgeerts scale is shown in Table 2. Patients without or with low endoscopic recurrence (i0 or i1 grade; 19 patients [41.30%]) were significantly more frequent in the LAP group than in the Open group (14/24 [58.33%] versus 5/22 [22.73%], respectively; P=.019).

Table 2.

Endoscopic and Clinical Recurrence After Ileocolic Resection for Crohn's Disease

	LAP (n=28)	Open (n=34)	P
Complete postoperative ileocolonoscopy	24 (85.71%)	22 (64.71%)	.082
Endoscopic Rutgeerts scale
i0	6	2	.247
i1	8	3	.171
i2	5	10	.116
i3	4	7	.307
i4	1	0	1
i0+i1/≥i2	14/10	5/17	.019^a
Clinical recurrence
First postoperative year	9	9	.779
At the end of follow-up	14	19	.799

Significant difference.

LAP, laparoscopic group.

Clinical recurrence was observed in 8 patients in the LAP group and 4 patients in the Open group (28.57% and 11.76%, respectively) (P=.116) 1 year after surgery and in 14 (50%) and 19 (55.88%) patients, respectively (P=.799), at the end of follow-up. Rates of clinical recurrence at 3 years (Fig. 1) were similar in the LAP and Open groups (52.6% versus 51.2%, respectively; P=.23) with a median delay for recurrence at 3.06 and 4.37 years, respectively. During the first postoperative year, medical treatment was comparable in both groups, with use of IS in 12 patients (5 patients in the LAP group) and anti-TNFα in 4 patients (1 patient in the LAP group). No patient required further bowel resection for CD during follow-up.

FIG. 1.

Clinical recurrence after laparoscopic (LAP group) or open (OPEN group) ileocolic resection for Crohn's disease in 62 patients.

Discussion and Conclusions

This study suggests that, at the era of IS and anti-TNFα, endoscopic recurrence seems less severe after laparoscopic ileocolic resection than after the conventional open procedure. However, these endoscopic findings do not seem to be related to better short- and mid-term clinical outcome. Additionally, our results support that the proposal even though the postoperative course is comparable after both approaches, laparoscopy allows a shorter hospital stay.

Regarding sex and age, our study's population is representative of the general population with CD. If the disease typically affects women 20%–30% more frequently, this higher incidence in women is not observed everywhere. In Europe and North America, male incidence increased, becoming equal and sometimes superior to female incidence,²⁰ as observed here. The LAP and Open groups were comparable in terms of sex, age, monitoring and indication for surgery, and previous medical treatments. Regarding the duration of the disease before the need for surgery our cohort is quite consistent with other French studies. A retrospective multicenter French survey conducted in 2006 on 90 patients showed a mean disease duration of 8.3±7 years between onset of symptoms and ileocolic resection.²¹ Regarding use of IS and anti-TNFα in recent studies, our population matches those of most reported recent studies.²²

Postoperative recurrence is common in patients with CD. Within 1 year postoperatively, clinical recurrence appeared in 10%–38% of patients, whereas endoscopic recurrence rates appeared in 48%–93% of patients.²³ As reported by Buisson et al.,⁴ in randomized controlled trials, approximately one-quarter of patients experienced clinical postoperative recurrence during the first year after surgery, whereas more than half of patients experienced endoscopic recurrence. Indeed, recurrent disease is initially characterized by subclinical endoscopic lesions preceding the development of clinical symptoms, and the endoscopic state of the neo-terminal ileum during the first year after surgery is the most powerful variable determining outcome.^18,24 To our knowledge, very few studies have compared recurrence rates after laparoscopic versus conventional surgery for CD,^25,26 and our study is the largest to compare endoscopic recurrence after laparoscopic or conventional ileocolic resection. In our experience, 12 of 62 (19.35%) patients experienced a clinical recurrence at 1 year, when 27 of 46 (58.69%) of them already had endoscopic lesions graded ≥i2; these results are consistent with the literature.^27,28 The main result of our study is that patients without or with low endoscopic recurrence (i0 or i1 grade) are significantly more frequent in the LAP group than in the Open group. Results of several studies favor a lesser immune and inflammatory response after gastrointestinal laparoscopic surgery compared with open surgery.^9,10,29 In the case of an inflammatory disease such as CD, this hypothesis might explain our results suggesting that endoscopic recurrence seems less severe after the laparoscopic approach (P=.019). However, these articles are mainly based on cancer surgery, and none has concerned patients with CD. Several teams have compared short- and long-term clinical outcomes in laparoscopy and conventional surgery in CD: in agreement with our results, all failed to demonstrate any difference for clinical recurrence rate after both approaches.^11,30

In our series, the postoperative period was uneventful for 51 patients (82.26%), without a difference between the LAP and Open groups, in both complication rates and severity of complications. These figures are consistent with the literature: most studies do not report any difference in postsurgical complications between both approaches, although some controlled studies have reported a reduced number of wound infections or postoperative small bowel obstruction with laparoscopic surgery.³¹ Despite an objective influence on postoperative morbidity, laparoscopy seemed, in our study as in others, to shorten the hospital stay.

Some limitations have to be acknowledged. First, the retrospective analysis of a prospective database might have introduced bias in analysis of medical records. Second, the sample size was relatively small, and repartition of patients changed in the study period, with a significant increase in number of laparoscopic procedures. Third, at the beginning of the study, laparoscopy was likely offered to healthier patients, but with increasing experience this approach was also offered to patients with complex disease. No significant preoperative difference was found between the LAP and Open groups; factors such as duration of CD prior to surgery, perianal disease, penetrating behavior, and pre- and postoperative medical treatments suspected to influence postoperative recurrence^32,33 were comparable in both groups.

In conclusion, this study suggests that, after ileocolic resection for CD, endoscopic recurrence seems less important after laparoscopic surgery than after laparotomy. These endoscopic findings precede clinical recurrence, which does not appear to be related to the surgical approach. Postoperative outcomes are comparable with both techniques, but laparoscopy shortens the hospital stay. For these reasons, laparoscopic ileocolic resection should be preferred to conventional surgery in patients with CD, but further wide-scale studies on surgical risk factors for postoperative endoscopic and clinical recurrence at the era of IS and anti-TNFα seem necessary.

Footnotes

Disclosure Statement

No competing financial interests exist.

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