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The American Journal of (2011) 201, 411–415

Midwest Surgical Association Incidence of small after laparoscopic and open colon resection

Melissa Alvarez-Downing, M.D.a, Zachary Klaassen, M.D.a,b, Robert Orringer, M.D., F.A.C.S.a, Mark Gilder, M.D., F.A.C.S.a, Debra Tarantino, M.D., F.A.C.S.a, Ronald S. Chamberlain, M.D., M.P.A., F.A.C.S.a,b,c,* aDepartment of Surgery, Saint Barnabas Medical Center, Suite 1172, 94 Old Short Hills Road, Livingston, NJ 07039, USA; bSt. George’s University School of Medicine, Grenada, West Indies, USA; cDepartment of Surgery, University of Medicine, Dentistry of New Jersey, Newark, NJ, USA

KEYWORDS: Abstract Small bowel BACKGROUND: Small bowel obstruction (SBO) is responsible for more than 1 billion dollars in health obstruction; care costs yearly in the United States. We sought to evaluate whether laparoscopic colorectal surgery resulted Colorectal resection; in a decreased incidence of SBO within the first year of surgical resection compared with open surgery. Laparoscopic surgery; METHODS: From January 2003 to December 2008, 339 patients underwent open (open colorectal Adhesion resection [OPEN]) colorectal resection and 448 patients underwent laparoscopic (laparoscopic colo- rectal resection [LAP]) colorectal resection. Hospital admissions up to 1 year after the initial resection identified patients admitted for the management of SBO, ileus, or nausea and vomiting. RESULTS: During the 1st year after surgery, 6 patients in the OPEN group developed SBO, and 5 patients in the LAP group developed SBO. The overall frequency of SBO for the OPEN group was 1.8% and 1.1% for the LAP group (P Ͻ .5461). CONCLUSIONS: Although advantages such as quicker postoperative recovery and decreased hos- pital stay have been attributed to laparoscopic surgery, no difference in the incidence of SBO within the 1st year of surgery was found compared with open colorectal surgery. © 2011 Elsevier Inc. All rights reserved.

Small bowel obstruction (SBO) is responsible for more for pelvic dissection4 with documented SBO rates as high as than 1 million inpatient hospital days and over 1 billion 10%.5 dollars in health care costs yearly in the United States.1 Since the introduction of laparoscopic surgery to treat Intra-abdominal adhesions form in 95%2 of patients under- both benign and malignant colorectal diseases, numerous going open abdominal surgery and are the cause of approx- authors have shown safe and equivalent resection and post- 3 imately 70% of SBO. Colorectal surgery has been con- operative outcomes using the laparoscopic approach.6 Fur- sidered an area of considerable risk for developing thermore, the introduction of hand-assisted laparoscopic postoperative SBO because in part of the frequent need resection to shorten operative times has further diversified a surgeon’s options when performing resection. Whether * Corresponding author: Tel.: ϩ1-973-322-5195; fax: ϩ1-973-322- laparoscopic resection results in decreased tissue manipula- 2471. tion, decreased adhesion formation, or specifically a de- E-mail address: [email protected] 3 Manuscript received June 15, 2010; revised manuscript September 8, creased incidence of SBO remains unclear. Duepree et al 2010 evaluated the incidence of SBO in 716 patients undergoing

0002-9610/$ - see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.amjsurg.2010.09.015 412 The American Journal of Surgery, Vol 201, No 3, March 2011 either laparoscopic or open colorectal resection. The authors Three hundred thirty-nine patients (43.1%) formed the reported a significantly lower incidence of admission for OPEN cohort, and 448 patients (56.9%) formed the LAP SBO in the laparoscopic group (1.9%) compared with the cohort. These patients were analyzed for the incidence of open resection group (6.1%); however, there was no signif- SBO (admission, hospitalization or surgery) in the subse- icant difference between the groups in regards to the inci- quent 12 months after their colorectal procedure. The mean 3 dence of SBO requiring surgical intervention. age in the OPEN group was 68.7 Ϯ 14.8 years versus In the current study, we analyzed a 5-year period of colo- 64.8 Ϯ 14.6 years in the LAP group (P Ͻ .002). The rectal resections that included predominantly open surgery at male-to-female ratio in the OPEN group was 231 male to the beginning of the study and primarily laparoscopic resection 217 and 150 to 189 in the LAP group (P Ͻ .0440). at the end of the study period. We sought to evaluate if The most common procedure performed in both laparoscopic colorectal surgery resulted in a decreased inci- groups was segmental , which included 277 dence of admission and treatment of SBO within the first year (81.7%) in the OPEN group and 408 (91.1%) in the LAP of surgical resection compared with an open approach. group. The segmental consisted of low an- terior resection (LAR) (127 OPEN and 203 LAP), right hemicolectomy (104 OPEN and 133 LAP), left hemico- Methods lectomy (16 OPEN and 42 LAP), sigmoidectomy (23 OPEN and 19 LAP), transverse colectomy (4 OPEN and A retrospective analysis of all consecutive patients, with 8 LAP), proctectomy (3 OPEN), and cecectomy (3 LAP). or without a previous history of abdominal surgery, under- The second most common procedure was subtotal colec- going elective open (open colorectal resection [OPEN]), tomy (14 OPEN, 4.1%; 24 LAP, 5.4%) followed by laparoscopic, or hand-assisted laparoscopic (laparoscopic abdominoperineal resection (APR) (22 OPEN, 6.5%; 4 colorectal resection [LAP]) colon resection between Janu- LAP, .9%) and total colectomy (16 OPEN, 4.7%; 9 LAP, ary 2003 and December 2008 was performed. Patients 2.0%). In the LAP group, hand-assisted cases accounted undergoing segmental colectomy (right or left), total colec- for 185 of the 203 (91.1%) LARs, 12 of 133 (9.0%) right tomy/proctocolectomy, or ileocolectomy were included. All hemicolectomies, 3 of 42 (7.1%) left hemicolectomies, 3 patients had a colorectal resection by 1 of 3 colorectal of 19 (15.8%) sigmoidectomies, 2 of 24 (8.3%) subtotal surgeons with a standard procedure and port placement. All colectomies, all 4 (100%) APRs, and 5 of 9 (55.6%) total open resections had a vertical midline incision. Patients who abdominal colectomies. There were significantly more underwent laparoscopic or hand-assisted laparoscopic re- LAP than OPEN segmental colectomies (P Ͻ .0002) and section had 3 to 5 trocar incisions ranging in size from 5 mm significantly more OPEN cases for APR (P Ͻ .0001), to 12 mm ports. The incision for the hand port was placed Ͻ infraumbilical in the midline. Any case converted to an open total abdominal colectomy (P .0395), and Hartmann’s Ͻ procedure (n ϭ 15) was counted as part of the OPEN cohort procedures performed (OPEN vs LAP) (P .0146). for the purpose of this study. There were 15 patients who were seen in the emergency The data collected included age, sex, index operation, and department or admitted to the hospital for nausea, vomiting, emergency room visit or hospitalization for SBO. SBO was paralytic ileus, or obstruction based on ICD codes. Subse- denoted based on admission codes for nausea and vomiting, quently, radiologic evaluation revealed mechanical SBO in ileus, or bowel obstruction. Subsequently, patients were further 5 patients (1.1%) in the LAP group (2 hand-assisted lapa- divided into 2 groups: (1) patients admitted with SBO that roscopy cases) and 6 patients (1.8%) in the OPEN group resolved with nasogastric decompression and conservative (Fig. 1). Among the LAP group, 3 patients with SBO were management and (2) patients treated surgically either urgently treated with conservative management, and 2 required sur- or because of failed nonoperative management (adhesiolysis or gical intervention. Among the 6 patients with SBO in the small bowel resection). Data for SBO were collected for 1 year OPEN group, 3 patients were treated conservatively and 3 after the initial surgical procedure. surgically. Three of 6 patients in the open group (50%) and All data are presented as mean values with standard 2 of 5 patients (40%) in the laparoscopic group with SBO deviation calculated using Microsoft Excel (Redmond, had abdominal surgery before their colorectal procedure, WA). Statistical analysis was completed using GraphPad with the most common being an . The initial Software (La Jolla, CA), and statistical significance was colorectal procedures performed in patients with SBO in the calculated using the Fisher exact test, with significance LAP group included 2 total colectomies (1 hand assisted) Ͻ defined as P .05. and 1 hand-assisted LAR, right hemicolectomy, and subto- tal colectomy. The colorectal procedures performed for pa- tients with SBO in the OPEN group included 3 right hemi- Results colectomies as well as 1 each for APR, LAR, and sigmoidectomy. The mean age of patients experiencing From January 2003 to December 2008, a total of 787 SBO in the LAP group was 65 Ϯ 18 years versus 68 Ϯ 15 patients underwent colorectal resection at our institution. years in the OPEN group (P Ͼ .05). Alvarez-Downing et al. Small bowel obstruction 413

Figure 1 The incidence and treatment of SBO for open and laparoscopic colorectal resection.

Comments found that within 2 years of an open intestinal resection with anastomosis (ICD-9 code 45) 14% of patients (1,057 of Each year in the United States, SBO is responsible for 7,393) had obstruction with 2.6% requiring adhesiolysis. In more than 300,000 hospital admissions, totaling over 1 a separate group of 6,765 patients undergoing other opera- million inpatient hospital days, and over 1 billion dollars in tions on the intestine (ICD-9 code 46), 17% of patients had 1 health care costs for hospitalization and physician services. obstruction, and 3.1% required adhesiolysis. Among pa- Intra-abdominal adhesions are the most common cause of tients undergoing rectal, rectosigmoid, or perirectal opera- SBO in the United States with an estimated frequency of tions (ICD-9 code 48), 15.3% had obstruction, and 5.1% of approximately 70%.7 Autopsy studies by Weibel and 8 patients required adhesiolysis within the same 2-year time Majno reported an incidence of intra-abdominal adhesions period.7 of 67% in patients undergoing abdominal surgery, whereas The incidence and risk of SBO after laparoscopic Menzies and Ellis2 reported an incidence as high as 93%. procedures in comparison with is undeter- Studies have estimated the risk of SBO after appendectomy mined. Reissman et al11 performed 100 laparoscopic and and at 1% to 10% and 10% to 25% after laparoscopic-assisted colorectal procedures and identi- any intestinal surgery.7,9 Colon and rectal surgery represents fied only 1 patient who developed SBO. Rosin et al12 one of the highest risk surgical procedures for developing performed 306 laparoscopic colorectal procedures over 8 adhesions and subsequent SBO, and reports have placed the incidence of SBO after colorectal surgery at 15% to 30%.2,9 years with a mean follow-up of 38 months. In their Three large studies have analyzed the incidence of SBO cohort, 6 patients developed SBO although 2 patients had after open colorectal procedures.7,9,10 Nieuwehuijzen et al9 previous open surgery, resulting in 4 patients (1.3%) with reported on 234 patients who underwent total or subtotal SBO directly related to their previous laparoscopic sur- 6 colectomy between 1985 and 1994 and identified SBO in gery. Sonoda et al analyzed the incidence of SBO after 18% of patients because of adhesions. Parker et al10 ana- colorectal resection among 266 patients undergoing lyzed 12,584 patients from the Scottish National Health hand-assisted laparoscopic surgery (HALS) versus 270 Service medical record linkage database undergoing open patients undergoing standard laparoscopic surgery (SLS). lower abdominal surgery in 1986 and found that 643 of Patients undergoing HALS resection did not statistically 8,861 (7.3%) readmissions were directly related to adhe- differ from patients who underwent SLS resection in sions. This included 430 patients (66.9%) requiring adhesi- terms of SBO incidence (4.1% vs 7.4%, P Ͻ .11). The olysis ( initial site of surgery, 64 patients; colon authors concluded that HALS does not lead to a higher initial site of surgery, 133 patients) and 197 patients incidence of SBO when compared with SLS for resec- (30.6%) requiring no operative treatment (rectum initial site tions of the colon and rectum.6 of surgery, 33 patients; colon initial site of surgery, 58 Duepree et al3 published the largest study on the inci- patients).10 Beck et al7 analyzed a random sample of Medi- dence of SBO after either laparoscopic bowel resection or care patients undergoing abdominal surgery in 1993 and open bowel resection. These authors reported on 211 pa- 414 The American Journal of Surgery, Vol 201, No 3, March 2011

Table 1 Recent published studies on the incidence and/or treatment of SBO for laparoscopic colorectal surgery including studies comparing LAP with OPEN

Patients Mean SBO incidence P SBO (conservative SBO (surgical Follow-up (N) age (y) Sex (M:F) (N) (%) value treatment) treatment) (%) (y) Current Study OPEN 339 68.7 150:189 6 (1.8) .54 3 (.9%) 3 (.9) 1 LAP 448 64.8 231:217 5 (1.1) 3 (.6%) 2 (.4) 1 Duepree3 OPEN 505 57.7 255:250 39 (7.7) .03 31 (6.1%) 8 (1.6) 2.42 LABR 211 50.8 91:120 7 (3.3) 4 (1.9%) 3 (1.4) 2.71 Rosin12 LBR 306 63 176:130 6 (2.0) N/A 5 (1.6%) 1 (.3) 3.17 Sonoda6 Hals 266 56 152:114 11 (4.1) .14 5 (1.9%) 6 (2.3) 2 SLS 270 58 127:143 20 (7.4) 7 (2.6%) 13 (4.8) 2.8 Previous studies analyzing the incidence of SBO after colorectal surgery show that OPEN and LAP results vary marginally. The results of the current study are in line with previous published studies, reporting that there is minimal advantage to OPEN over LAP procedures. M ϭ male; F ϭ female; NA ϭ not applicable.

tients who underwent laparoscopic-assisted bowel resection when compared with patients undergoing open colorectal (LABR) and 505 patients who underwent open bowel re- resection. Interestingly, 60% (n ϭ 3) of SBO in LAP pa- section (OPEN), with a mean follow-up period of 2.71 and tients occurred in patients having a total colectomy. In- 2.42 years, respectively. They reported that SBO requiring creased bowel manipulation and dissection associated with conservative treatment was significantly less in the LABR a total colectomy may increase a patient’s risk of SBO patients (n ϭ 4) compared with the OPEN patients (n ϭ 31) compared with other colorectal resections. However, (P Ͻ .016). Furthermore, there was no significant difference breaching the peritoneal barrier, even with minimally inva- in surgical intervention for patients with SBO (LABR 3 sive incisions and laparoscopic intracorporeal manipulation patients, OPEN 8 patients).3 The authors concluded that of abdominal organs, predisposes patients to postoperative minimally invasive procedures for bowel resection resulted adhesions and potential SBO that is not unlike traditional in a significant decrease in the incidence of postoperative open surgery. Although colorectal surgery continues to SBO. evolve into a minimally invasive discipline, the difficult In the current study of 787 patients, including 339 clinical issue of postoperative SBO is not ameliorated with OPEN patients and 448 LAP patients, we identified a laparoscopic colorectal surgery. 1.8% incidence of SBO within the first year of surgery for OPEN patients and 1.1% for LAP patients (P Ͼ .05). A 1-year timeframe was chosen because the incidence of References SBO after colectomy is well documented (Ͼ25%), with ϳ58% of all SBO occurring within the first year.10 Of 1. Ray NF, Denton WG, Thamer M, et al. Abdominal adhesiolysis: note, this SBO incidence is comparable to results re- inpatient care and expenditure in the united States in 1994. J Am Coll 12 ported by Rosin et al (5 patients treated conservatively, Surg 1998;186:1–9. 1.6%; 1 patient treated surgically, .3%) and Sonoda et al6 2. Menzies D, Ellis H. Intestinal obstruction from adhesions—how big is (7 patients treated conservatively, 2.6%; 13 patients the problem? Ann R Coll Surg Engl 1990;72:60–3. treated surgically, 4.8%) despite a longer follow-up pe- 3. Duepree HJ, Senagore AJ, Delaney CP, et al. Does means of access affect the incidence of small bowel obstruction and ventral after riod (3.17 and 2.8 years, respectively). Acknowledging bowel resection? versus laparotomy. J Am Coll Surg 3 that our results are in contrast to those of Duepree et al 2003;197:177–81. in regards to the incidence of SBO between laparoscopic 4. Indar AA, Efron JE, Young-Fadok TM. Laparoscopic ilieal pouch-anal and open colorectal resection, it is noteworthy that sim- anastomosis reduces abdominal and pelvic adhesions. Surg Endosc ilar to Duepree et al and others3,6,12 we found no differ- 2009;23:174–7. 5. Parikh JA, Ko CY, Maggard MA, et al. What is the rate of small bowel ence in the treatment outcomes or approach to SBO obstruction after colectomy? Am Surg 2008;74:1001–5. between the laparoscopic and open groups (Table 1). 6. Sonoda T, Pandey S, Trencheva K, et al. Longterm complications of This is the first study to compare the incidence of SBO hand-assisted versus laparoscopic colectomy. J Am Coll Surg 2008; within the 1st year of surgery for patients undergoing lapa- 208:62–6. roscopic or open colorectal resections. Although laparo- 7. Beck DE, Opelka FG, Bailey HR, et al. Incidence of small-bowel obstruction and adhesiolysis after open colorectal and general surgery. scopic surgery has numerous well-documented advantages, Dis Colon Rectum 1999;42:241–8. laparoscopic colorectal resection did not significantly de- 8. Weibel MA, Majno G. Peritoneal adhesions and their relation to crease the incidence of SBO within the 1st year of surgery abdominal surgery. Am J Surg 1973;126:345–53. Alvarez-Downing et al. Small bowel obstruction 415

9. Nieuwenhuijzen M, Reijnen MM, Kuijpers JH, et al. Small bowel It was not involved in the analysis of the study because of obstruction after total or subtotal colectomy: a 10-year retrospective inconsistent numbers between the 3 surgeons. To answer review. Br J Surg 1998;85:1242–5. 10. Parker MC, Ellis H, Moran BJ, et al. Postoperative adhesions: ten-year your second question, I probably would include a reference follow-up of 12,584 patients undergoing lower abdominal surgery. Dis to the Sonota study from 2009, which looked at about 500 Colon Rectum 2001;44:822–9. patients undergoing hand-assist or standard laparoscopic 11. Reissman P, Cohen S, Weiss EG, et al. Laparoscopic colorectal sur- surgery. There were 20 patients with SBO in the standard gery: ascending the learning curve. World J Surg 1996;20:277–81. laparoscopic group and 11 patients in the hand-assisted 12. Rosin D, Zmora O, Hoffman A, et al. Low incidence of adhesion- related bowel obstruction after laparoscopic colorectal surgery. J Lapa- group. Roughly 50% in both groups were surgically treated. roendosc Adv Surg Tech A 2007;17:604–7. So, based on our small numbers and their data, I would say that hand-assist does not lead to increased frequency of surgical treatment of SBO. To answer the third question, it Discussion would be interesting to extend the study past 2 years and to examine the film issue. Akpofure Peter Ekeh, M.D. (Dayton, OH): Are you Harry L. Reynolds Jr, M.D. (Cleveland, OH). First, just as laparoscopic techniques have been proposed as useful in certain that all the patients that were operated on had pro- decreasing adhesion formation, multiple products have been cedures in your hospital? Could they have gone to sur- developed to be used intra-abdominally to prevent adhe- rounding hospitals with their complications? And, the sions. Were any of the hyaluronic acid-based adhesion pre- second question, did you take into account the possibility vention products used in either the open laparoscopic or that some of these patients may have had previous ab- assist cases, and, if so, was this evaluated in the analysis? dominal surgery, which might bias your incidence of Second, I noted the authors used hand-assist techniques in a bowel obstruction? significant number of these patients. Like the authors, I have Dr. Klaassen: There is no way to be certain if these found hand-assist techniques useful, but I am frequently patients did come back to our hospital or go to another accused by my partners of performing open surgery when I hospital, but we are a community hospital in a suburban place a hand in the abdomen. The 2 lap patients who New York area, so most of patients would come back to our developed bowel obstruction and required surgery were in hospital. To answer your second question, there were 3 the hand-assist group. The numbers are small, but do you patients in the open group and 2 patients in the laparoscopic think there is any significance to the observation that the group who had prior abdominal operations. hand-assist laparoscopic cases with obstruction were oper- Christopher P. Brandt, M.D. (Cleveland, OH): In the ated while the 3 straight laparoscopic cases were managed patients who were treated surgically for SBO, were those medically? And, finally, do you plan on carrying out the operations done laparoscopically or open? And, would it be analysis longer, perhaps breaking out the hand-assist cases more likely you could accomplish it laparoscopically in as a separate group and seeing if there is a difference that people who had a laparoscopic versus an open procedure? develops over an extended period? Dr. Klaassen: Of the 5 patients treated surgically, 4 Zachary Klaassen, M.D. (Livingston, NJ): To answer were exploratory , and 1 was a diagnostic lap- your first question, hyaluronic acid film is the prevention aroscopy. I do agree that if a patient initially had a laparo- product of choice for surgeons at our hospital. Of the 3 scopic procedure, it would be at least nice to try a diagnostic surgeons that were involved in the study, 1 routinely uses it. laparoscopy first.