The Extent and Severity of Adhesions Are Reduced After Major Laparoscopic Colorectal Surgery: A Pilot Study

Abstract

Background:

Adhesion formation after colorectal surgery is a well-recognized problem, and the ability of the laparoscopic technique to reduce adhesion formation is questionable. The present study compares adhesion formation after laparoscopic and open colorectal surgery.

Patients and Methods:

A diagnostic laparoscopy was performed through the stoma site at the ileostomy closure operation in patients who had undergone low anterior resection or ileal pouch anal-anastomosis. The laparoscopy was videorecorded, and the extent and severity of adhesions involving incisions, omentum, small bowel, and female adnexa were graded.

Results:

Twenty-three patients were enrolled into the study, and after exclusions 19 patients remained for the analyses. There was no difference in baseline characteristics of patients except in the mean (range) total incision length, which was 22 (21–23) cm in the open group and 10.9 (9–14) cm in the laparoscopic group (P < .001). The median (range) overall adhesion severity score was 7 (3–9) in the open group and 0 (0–4) in the laparoscopic group (P = .001). Similar differences were seen in overall extent and total score (P = .001 and P = .001, respectively). In detailed analysis, incision and small bowel adhesions scores were also statistically significantly different, favoring laparoscopic surgery.

Conclusions:

According to the present study, although low in number of patients, laparoscopic colorectal surgery may result in fewer adhesions compared with open surgery.

Introduction

Postoperative intraabdominal adhesion formation is a well-known sequel of abdominal surgery. It has been estimated that up to 97% of patients develop adhesions after major open abdominal procedures.¹ The clinical burden of adhesion-related hospital re-admissions is enormous,² and the economic impact of adhesive small bowel obstruction is significant as shown by recent epidemiological studies.^3,4 Moreover, adhesions may cause female infertility and contribute to abdominal or pelvic pain.⁵ They also prolong abdominal opening time and put patients at high risk for inadvertent enterotomy.^6,7

The complexity of adhesion prevention after laparotomy has been addressed by a recent review.⁸ In general, commonly presented advice is that trauma to the peritoneal surface should be minimized during surgery. This includes principles such as gentle tissue handling, meticulous hemostasis, limited dissection, and avoiding spillage of intestinal contents. The laparoscopic technique fulfills well most of these principles and could potentially reduce adhesion formation. Previous studies have suggested that laparoscopy reduces adhesions in gallbladder and gynecologic surgery.^9,10 As the technique has many advantages over its open counterpart regarding postoperative recovery, the use of it has been adopted widely also in colorectal surgery. Procedures on the colon and rectum have been classified as high-risk surgery in terms of adhesion formation. It would be beneficial for patients if the amount of adhesions would be diminished with the use of that mini-invasive technique. After years of usage of laparoscopy in colorectal operations, the issue is still debatable because recent reviews end up with conflicting conclusions.^11–13

The aim of the present study was to clarify the issue by comparing adhesion formation in open and laparoscopic major colorectal surgery. The primary goal was to evaluate adhesion severity and extent on incision, omentum, and small bowel. The secondary aim was to evaluate female genital adhesions.

Patients and Methods

A prospective study was undertaken in order to compare adhesion severity and extent in patients operated on laparoscopically and openly. All patients scheduled for low anterior resection (LAR) or ileal pouch anal-anastomosis (IPAA) operation with covering ileostomy were prospectively screened for the study. After written consent was obtained, patients were enrolled into the study. The initial operation was performed on a routine basis by or under the supervision of the author except for one laparoscopic LAR. At the second operation a diagnostic laparoscopy was undertaken through the stoma site.

The study was approved by the ethics committee of the Päijät-Häme Social and Health Care Group (PHSOTEY Dnro ETMK25/2009).

Surgical technique

LAR operations were performed using radical surgical principles. In laparoscopic operations the inferior mesenteric vein was first dissected free proximally and divided by the vessel-sealing technique (Ligasure™; Valleylab, Boulder, CO). The descending colon was medially mobilized until the approximate level of the inferior mesenteric artery. After that, dissection was continued from the promontory upward until the inferior mesenteric artery was clearly exposed. The artery was ligated at the high position by the vessel-sealing instrument. Dissection was then continued downward using total mesorectal excision principles. All the dissection was done by the vessel-sealing instrument. The splenic flexure was mobilized when necessary. A left lower abdomen muscle-splitting incision was used to exteriorize the bowel. In open LAR operations the same oncological principles were used. The midline incision was used to enter the abdomen. Inferior mesenteric vessels were handled beginning either distally or proximally depending on the patient using the vessel-sealing instrument.

All IPAA operations were performed laparoscopically beginning from the right colon. Mobilization of the colon and ligation of the arteries were performed by the vessel-sealing technique. The omentum was saved. A right lower abdomen muscle-splitting incision was used to exteriorize the bowel. At the reversal operation the loop ileostomy was closed by a linear stapler, and the bowel was replaced in the abdomen. The opening of the stoma site was closed in part, and a laparoscopic trocar was inserted. An additional 5-mm port was inserted to facilitate the inspection of abdominal organs, and diagnostic laparoscopy was performed. The laparoscopic phase of the operation was videorecorded for later grading of adhesions.

Adhesion scoring system

The severity and extent of adhesions were scored by a modified system presented by Dowson et al.¹⁴ and Hull et al.¹⁵ The grading system is shown in Table 1. The scoring was performed gradually in the following order: adhesions to surgical incisions, other adhesions involving omentum, and other adhesions involving small bowel. By this system any adhesion was scored only once. Adhesions involving the Fallopian tubes and ovaries were scored separately in female patients. The adhesion scoring was focused on these sites because they are regarded as important in the development of adhesive obstruction and female infertility. Adhesions found in the primary operation were noted, and only newly formed adhesions were graded in the reversal operation.

Table 1.

The Adhesion Scoring System

Score	Extent	Severity
0	No adhesions	No adhesions
1	Covering up to 25% of total area/length	Filmy, avascular adhesions
2	Covering 26%–50% of total area/length	Moderately thick adhesions, separated mostly by blunt dissection
3	Covering 51%–75% of total area/length	Dense adhesions separated only by sharp dissection
4	Covering 76%–100% of total area/length

Statistical analysis

Continuous variables are presented as mean or median (range) values. The statistical significance of continuous variables with normal distribution was tested by analysis of variance. The comparison of adhesion scores was performed by the Mann–Whitney U test using the null hypothesis that there would be no difference between groups. Categorical variables were compared by chi-squared test. A value of P < .05 was considered as statistically significant. Statistical analysis was performed using SPSS version 20.0 for Windows software (SPSS, Chicago, IL).

Results

Altogether, 23 patients consented and were enrolled into the study. Two patients in the open group suffered from local pelvic infection after the initial operation. Four patients were excluded for the following reasons: 3 had no laparoscopy during the reversal, and 1 patient had to be operated on due to stoma-related obstruction. The study population consisted of the remaining 19 patients. There were 12 male and 7 female patients. LAR was performed on 17 patients, and laparoscopic IPAA was performed on 2 patients (both men).

Two patients in the open (50%) and 4 patients (26.7%) in the laparoscopic group received anti-adhesive agent (Sprayshield™; Covidien, Waltham, MA) at the end of the initial operation in order to prevent adhesions to the omentum, pelvis, and main incision. They were, however, included in the analysis because otherwise the number of patients would be very low.

There were no statistically significant differences between the groups regarding the T-grade of the tumor and preoperative radiation (data not shown). There were two anastomotic leakages resulting in pelvic infection in the open group. The infection remained local in both cases, and no patients in the present series suffered from intraabdominal infection.

Baseline characteristics of the patients are shown in Table 2. The only statistically significant difference between the laparoscopic and open groups appeared in the length of the incision (P < .001).

Table 2.

Baseline Characteristics of Patients

	Laparoscopic group (n = 15)	Open group (n = 4)	P value
Gender (male/female)	8/7	4/0	.086^a
Age (years)	66.6 (50–81)	65.8 (59–72)	.851^b
BMI (kg/m²)	27.3 (22.2–37.7)	27.6 (23.0–34.6)	.897^b
ASA (score)	2 (1–3)	2 (2–3)	.810^c
Incision length (cm)	10.6 (9–14)	22 (21–23)	<.001^b
Reversal interval (days)	110.9 (43–290)	254.5 (71–715)	.101^b

Data are number of patients or mean or median (range) values as appropriate.

By chi-squared test.

By analysis of variance.

By Mann–Whitney U test.

ASA, American Society of Anesthesiologists; BMI, body mass index.

The comparison of overall median adhesion scores between the laparoscopic and open groups is shown in Table 3. All the differences between the laparoscopic and open groups were highly significant.

Table 3.

The Median of Severity, Extent, and Total Adhesion Scores

Score	Laparoscopic group	Open group	P value
Severity	0 (0–4)	7 (3–9)	.001
Extent	0 (0–2)	5.5 (3–7)	.001
Total	0 (0–6)	12 (7–16)	.001

Data are median (range) values. The statistical analysis has been performed by Mann–Whitney U test.

The detailed analysis of adhesion scores in different anatomical sites is shown in Table 4. There was a statistically significant difference between the laparoscopic and open groups in small bowel and incision adhesion scores.

Table 4.

Detailed Analysis of Adhesion Scores According to Anatomic Site

	Laparoscopic group	Open group	P value
Incision
Severity	0 (0–2)	2 (0–3)	.037
Extent	0 (0–1)	3 (0–4)	.027
Omentum
Severity	0 (0–2)	2.5 (0–3)	.049
Extent	0 (0–1)	1 (0–1)	.100
Small bowel
Severity	0 (0–2)	2 (1–2)	.009
Extent	0 (0–1)	1 (1–2)	.006

Data are median (range) values. The statistical analysis has been performed by Mann–Whitney U test.

Table 5 shows the severity and extent of adnexal adhesions in female patients.

Table 5.

Severity and Extent of Tubal and Ovarial Adhesions in Female Patients

	Severity/extent
	Left		Right
Patient	Tube	Ovary	Tube	Ovary
I	2/1	0/0	0/0	0/0
II	0/0	0/0	0/0	0/0
III	0/0	0/0	0/0	0/0
IV	0/0	0/0	0/0	0/0
V	0/0	0/0	0/0	0/0
VI	0/0	0/0	0/0	0/0
VII	0/0	1/1	0/0	1/1

There were 5 female patients (I–VII) in the study. All patients had low anterior resection for cancer.

Discussion

Open colorectal surgery has been classified as high-risk surgery regarding adhesion-related hospital re-admissions.^2,16 Furthermore, after open IPAA operation, adhesion-related small bowel obstruction may be as high as 40%, and the risk of infertility in female patients has been estimated to be threefold higher compared with medically treated ulcerative colitis patients.^17,18 The need for methods that reduce adhesion formation is evident. Laparoscopic surgery, being atraumatic, and the mini-invasive technique could potentially fulfill the need. However, the role of laparoscopy in decreasing adhesion formation and their clinical consequences are still debatable.^11–13

In the present study, both the extent and severity of intraabdominal adhesions were reduced after laparoscopic rectal cancer and IPAA surgery. It is also important that the reduction could be clearly seen in adhesions involving incisions and small bowel.

Our study is well in line previous studies having a similar or almost similar approach. Dowson et al.¹⁴ compared the amount of adhesions by diagnostic laparoscopy after a variety of open and laparoscopic colorectal procedures. Their primary end point was the overall adhesion score, and the secondary end point was adhesion formation at the main access incision. In comparison, between the open and laparoscopic groups there was a significant difference in both end points. A weakness of their study is that only one-quarter of the patients had a laparoscopic initial operation. Indar et al.¹⁹ found that laparoscopic IPAA resulted in few adhesions to the abdominal wall or to adnexae; they had no control group but compared their findings with previously published results obtained from open operations. The latest study by Hull et al.¹⁵ evaluated incisional, female genital organ and total abdominal adhesions scores by a prospective manner; in each evaluated score there was a statistically significant difference favoring laparoscopic surgery. Furthermore, two recent studies have shown that there are fewer peristomal adhesions and that closure of loop ileostomy is easier to perform after a laparoscopic initial operation.^20,21 It is noteworthy that all previous studies and the current one obtained uniform results.

Unfortunately, the number of patients in the current and previous studies is low. A large, randomized controlled study would give the most reliable answer regarding the issue. However, taken into account the clear short- and long-term benefits of the laparoscopic approach to patients, a randomized study could be regarded as unethical to carry out.

A detailed evaluation of adnexal adhesions was also carried out in the present study. It is noteworthy that 13 out of 14 Fallopian tubes and 12 out of 14 ovaries of females were totally free of adnexal adhesions after laparoscopic surgery. Furthermore, the 2 patients with adnexal adhesions had a limited amount of adhesions. According to the American Fertility Society classification of adnexal adhesions, the degree of their adhesions is classified as minimal. All women in the present study were operated on laparoscopically, and comparison with an open group could not be done. However, based on the present study it can be assumed that the risk of adnexal adhesions after laparoscopic LAR is minimal.

The current and previous studies clearly suggest that adhesion formation after laparoscopic surgery is reduced compared with open surgery. However, it is well known that many of the patients who have adhesions will remain symptom free. Thus, it is somewhat questionable if usage of the laparoscopic technique, with a certain reduction of adhesions, results in clinical benefits such as diminished incidence of small bowel obstruction or improved fertility.

The previous literature regarding the risk of small bowel obstruction after open or laparoscopic colorectal surgery is conflicting.^22–25 Part of this inconsistency may be related to the methodology of the studies. In randomized studies the statistical power has been inadequate, the conversion rate has been high, and analyses have been conducted using the intention-to-treat method. However, trends in the CLASICC-trial suggest that with a diminished conversion rate, a significant difference could be achieved favoring laparoscopic surgery.²²

Adnexal adhesions may contribute to female infertility.⁵ According to the present and previous studies, the extent and severity of tubal and ovarial adhesions are minimal after laparoscopic colorectal surgery and less than after open corresponding surgery. It is very probable that this is associated with clinical benefit because pregnancy rates have been shown to increase after laparoscopic IPAA.²⁶

Another important clinical issue is the risk of inadvertent bowel injuries in repeat surgery. A recent review by Ten Broek et al.²⁷ even suggests that the difficulties in re-operations impact most adhesion-related morbidity. An important finding of the SCAR-1 study was that the rate of re-operations potentially complicated by adhesions is roughly 40 per 100 initial operations.² The results of the present study strongly suggest that usage of a laparoscopic technique with a reduced amount of postoperative adhesions in colorectal surgery makes subsequent surgery easier and safer.

There are certain advantages of the present study compared with previous ones. The study was conducted prospectively, all procedures were performed with similar technique, and possible previous adhesions found during the initial operation were excluded. Another strength of the study is that the majority of patients had rectal resection because the clinical benefit of laparoscopy on this group of patients is more questionable compared with colon surgery.²²

The current study has some potential weaknesses. The number of patients is low, and the vast majority of patients were operated on laparoscopically. As the statistically significant difference was achieved with this low number of patients, it was regarded as useless and in part unethical to continue the study, although laparoscopy in the reversal operation is considered safe.

The low number of patients operated on by the open procedure reflects the current practice in our hospital. More than 80% of colorectal procedures are performed laparoscopically, and one could consider it unethical to do more open operations only for the purpose of the study.

One confounding factor in the present study is that 2 patients in the open group had pelvic infection after the initial operation. Pelvic inflammation is a potential inducer of adhesions involving the omentum or small bowel. In fact, this could be seen in 1 patient but not in the other with anastomosis leakage.

Diagnostic laparoscopy showed that the small bowel was attached to the pelvis by Grade 1–2 adhesions. These pelvic adhesions were neither graded nor included in the analysis. However, an additional statistical analysis including these showed still a significant difference favoring the laparoscopic technique.

Some patients received anti-adhesion agent during the first operation. These patients were included in the analyses. There are valid reasons not excluding these patients. The first was because of the low number of open operations and that Sprayshield was applied only to a restricted area in the abdomen. Furthermore, 50% of patients in the open but only roughly one-quarter of the patients in the laparoscopic group received the agent. Considering this, there should not been bias favoring the laparoscopic technique. Furthermore, a sensitivity analysis was performed including only patients without anti-adhesive treatment. The analysis showed similar findings in 10 out of 12 evaluated scores, although the power of the study decreased.

Conclusions

This prospective study, although low in number of patients, suggests that the laparoscopic technique reduces adhesion formation in major colorectal surgery. Further studies with larger numbers of patients is warranted to confirm the results obtained by the present study.

Footnotes

Disclosure Statement

No competing financial interests exist.

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