UvA-DARE (Digital Academic Repository) Clinical issues in the surgical treatment of colon cancer Amri, R. Link to publication
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1 UvA-DARE (Digital Academic Repository) Clinical issues in the surgical treatment of colon cancer Amri, R. Link to publication Citation for published version (APA): Amri, R. (2015). Clinical issues in the surgical treatment of colon cancer General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam ( Download date: 24 Dec 2017
2 Part III: Surgical Safety and Complications
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4 Chapter 10: The impact of adhesions on operations and postoperative recovery in colon cancer surgery Ramzi Amri Hannah C. den Boon Liliana G. Bordeianou Patricia Sylla David L. Berger American Journal of Surgery. 2013;206(2):
5 Chapter 10 Abstract Background Many surgeons assume that adhesions encountered during surgery negatively influence surgical outcomes. This article attempts to assess the role adhesions have on outcomes of colon cancer surgery. Methods Records of 1071 consecutive patients operated for colonic adenocarcinoma ( ) were reviewed. Patients were assigned to 3 groups: no adhesions, any adhesions, or dense adhesions. Multivariate regression assessed the association between adhesions and the duration of surgery and stay as well as laparoscopic conversion and complication rates. Results Adhesions were encountered in 329 (30.7%) patients; 138 (12.8%) had dense adhesions. After correction for age and comorbidities, having adhesions was associated with longer surgeries (P<0.001), longer hospital stays (P=0.029), a borderline significantly higher conversion rate (P=0.058), and a delayed return of bowel function (P=0.037). Dense adhesions had stronger associations with surgical duration (P<0.001), stay duration (P<0.001), and conversion (P<0.001). Conclusions Abdominal adhesions independently put patients at risk for a longer and more complicated perioperative stay after colon cancer surgery. 138
6 Impact of adhesions on surgery and recovery T he consequences of intra-abdominal adhesions encountered when performing colorectal surgery are difficult to quantify. Adhesions are a common surgical finding and have been reported to develop after up to 90% of major abdominal surgeries. 1 Reports estimate that between 14% 1,2 and up to 40% 3 of all bowel obstructions are related to adhesions. The risk of developing a small bowel obstruction related to adhesions after undergoing an open colectomy has been estimated at 9% 4 in previous literature. Adhesions are possibly a source of various intraoperative complications. In addition, adhesiolysis may cause a longer operative time, 5 may contribute to laparoscopic conversions, 6 and may lead to a longer postoperative stay. 7, 8 The clinical magnitude of adhesions is poorly researched, 7 and earlier research focused on the long-term complications caused by the formation of adhesions. In contrast, little is known about the risks for patients who have abdominal adhesions while undergoing colorectal surgery or, in particular, colon cancer patients. Patients who have dense adhesions may be particularly affected. The aim of this study is to investigate the role of (dense) adhesions in causing perioperative complications. Methods Patients Electronic and paper records for all patients operated on for colon cancer at Massachusetts General Hospital between January 1, 2004, and December 31, 2011, were reviewed. Patients were assigned to three groups: The first of these is the control group, which was formed by all patients without any intraoperative findings of adhesions. The second group comprised all patients who were reported to have adhesions. The third group includes only cases in which operative reports described extensively dense adhesions. Although the latter is essentially formed by reported observations during surgery, this approach is the only way to isolate the most stringent intraoperative adhesions for the lack of a systematically used objective score to use as a selection criterion. Tumor attachments to other structures and any other forms of tumor adherence were not considered to be adhesions. The main outcome measures were the duration of the operation, the conversion rate, the duration of stay, and 30-day postoperative morbidity and mortality. Secondary outcome measures were reoperation and readmission. The population was controlled for differences in baseline characteristics including age, race, sex, body mass index, American Society of Anesthesiologists (ASA) classification, and Charlson comorbidity score
7 Chapter 10 We also verified for any differences in smoking habits and the prevalence of symptomatic inflammatory bowel disease. Multivariate regression models were used to correct for any of the potential confounders caused by differences in baseline characteristics. Statistical analysis Statistical significance was assessed using the chi-square (χ 2 ) test or the Mann-Whitney U test for non-normally distributed variables and the t test for normally distributed variables. The Fisher's exact test was applied for binary outcomes with an expected frequency below 5. Multivariate analysis was performed using binary logistic and linear regression models for dependent variables that were binary and continuous, respectively. All analyses were performed using SPSS (IBM SPSS Statistics for Windows Version 20.0; IBM Corp, Armonk, NY); a P-value under 0.05 was considered statistically significant. Results From January 1, 2004, to December 31, 2011, 1071 patients underwent colon cancer surgery. Of those patients, 329 (30.7%) had intraoperative adhesions, and in 138 (12.8%) of these patients the adhesions were considered dense. The remaining 742 (69.3%) patients were not reported to have any adhesions. Population characteristics The baseline characteristics of the study population are shown in Table 1. Sex, race, or body mass index distributions were not significantly different. The presence of adhesions was related to age at the time of operation, with an increase of the mean age from 65 years in the absence of adhesions to 70.1 years in all patients with adhesions and 71.6 years in those with dense adhesions (P<0.001 for both). As expected, the presence of adhesions was strongly related to a history of abdominal surgery; 29.6% of patients without adhesions had previous abdominal surgery, whereas 72.3% of those patients with adhesions and 76.8% of those with dense adhesions (P<0.001 for both) had previous surgery. Patients with dense adhesions also had more comorbidities (mean Charlson comorbidity score of 3.29 vs. 3.19; P=0.009) and a higher ASA score (mean score=2.58 vs. 2.34; P<0.001). In the group including all patients with adhesions, only the ASA score was significantly higher (2.42 vs. 2.34, P=0.012). There were no significant differences in smoking rates and the number of patients with symptomatic inflammatory bowel disease (e.g., Crohn's disease or ulcerative colitis). 140
8 Impact of adhesions on surgery and recovery Table 1. Baseline population characteristics at surgery Adhesions None All P-value Dense P-value Total, N (%) 742 (69.3) 329 (30.7) (12.8) - Age, mean, years ± SD 65 ± ±12.4 < ±13 <0.001 BMI, mean, kg/m 2 ± SD 27.4 ± ± ± Race (white) (%) Sex (male) (%) Previous of abdominal surgery (%) < <0.001 Current smoking (%) History of smoking (%) Diagnosis of Crohn's disease (%) Diagnosis of ulcerative colitis (%) ASA score, mean, ± SD 2.34 ± ± ±0.58 <0.001 Charlson score, mean, ± SD 3.19 ± ± ± BMI = body mass index; SD = standard deviation. Surgery-related complications As seen in Table 2, the presence of adhesions led to longer operative times, increasing the mean duration of surgery from 128 to 164 minutes (P<0.001). The rate of conversion in laparoscopic and hand-assisted laparoscopic cases also increased from 10.8% at baseline to 19.3% in all adhesions (P=0.055) and 38.5% in dense adhesions (P<0.001). Table 2. Surgery characteristics None (n=742) All (n=329) Adhesions P-value Dense (n=138) P-value Surgery duration, minutes, mean ± SD 128 ± ±91 < ±92 <0.001 Conversion (laparoscopic and hand assisted) (%) <0.001 Conversion (laparoscopic only) (%) SD = standard deviation. The same pattern, albeit with lower statistical significance, appeared when excluding hand-assisted approaches. Conversion rates were 11.5%, 19.6% (P=0.14), and 36.8% (P=0.003), respectively. 141
9 Chapter 10 Postoperative stay and complications As shown in Table 3, adhesions contribute to a longer postoperative stay, adding approximately a day to the average stay (from 6.3 to 7.38 days [P=0.005]). In patients with dense adhesions, this mean difference in stay duration doubles to over 2 additional days with an average duration of 8.74 days (P<0.001). However, adhesions did not significantly increase mortality, readmission, or reoperation rates within 30 days of the operation. Table 3. Stay duration and complications None (n=742) All (n=329) Adhesions P-value Dense (n=138) P-value Stay duration (mean, days) 6.30 ± ± ±9.4 <0.001 In-stay death, N (%) 12 (1.6) 4 (1.2) (2.2) day readmission rate, N (%) 58 (7.8) 24 (7.3) (8.7) day reoperation rate, N (%) 19 (2.6) 10 (3) (5.1) 0.11 An evaluation of differences in all postoperative complications that could possibly relate to adhesions is shown in Table 4. The only significant difference found was an increase in the rate of prolonged or returning to nothing by mouth (NPO) status from 4.7% to 7.9% in patients with adhesions (P=0.038) and with a strong trend of 8.7% in those patients with dense adhesions (P=0.056). Table 4. Postoperative complication rates None (n=742) n (%) All (n=329) n (%) Adhesions P-value Dense (n=138) n (%) Prolonged ileus In-stay 6 (8.8) 38 (11.6) (6.5) 0.38 Post-release 6 (0.8) 2 (0.6) P-value Total 71 (9.6) 40 (12.2) (6.5) 0.25 Anastomotic leak In-stay 12 (1.6) 3 (0.9) (0.7) 0.43 Post-release 4 (0.5) 1 (0.3) 1 1(0.7) 0.58 Total 16 (2.2) 4 (1.2) (1.4) 1 Wound dehiscence In-stay 3 (0.4) 1 (0.3) 1 1(0.7) 0.5 Post-release 1 (0.3) 2 (0.6) (0.7) 0.29 Total 4 (0.5) 3 (0.9) (1.4) 0.48 Wound Infection In-stay 39 (5.3) 23 (7) (6.5) 0.55 Post-release 9 (1.2) 4 (1.2) 1 3(2.2) 0.42 Total 47 (6.3) 27 (8.2) (8.7)
10 Impact of adhesions on surgery and recovery Table 4. Postoperative complication rates (continued) None (n=742) n (%) All (n=329) n (%) P Adhesions Dense (n=138) n (%) Gastrointestinal Bleed In-stay 2 (0.3) 1 (0.3) 1 1 (0.7) 0.40 Post-release 3 (0.4) Total 5 (0.7) 1(0.3) (0.7) 1 ICU Transfer In-stay 22 (3) 12 (3.6) (5.1) 0.2 Post-release 1 (0.1) Total 23 (3.1) 12 (3.6) (5.1) 0.3 NGT replacement In-stay 68 (9.2) 39 (11.9) (10.1) 0.72 Post-release 8 (1.1) 1 (0.3) (0.7) 1 Total 76 (10.2) 40 (12.2) (10.9) 0.82 Unplanned TPN In-stay 15 (2) 6 (1.8) (2.2) 0.75 Post-release 7 (0.9) 3 (0.9) 1 1 (0.7) 1 Total 22 (3.0) 9 (2.7) (2.9) 1 Unplanned NPO In-stay 31 (4.2) 23 (7.3) (8.7) Post-release 4 (0.5) 2 (0.6) Total 35 (4.7) 26 (7.9) (8.7) Bowel perforation In-stay 3 (0.4) 2(0.6) (0.7) 0.5 Post-release 0 0 N/A 0 N/A Total 3 (0.4) 2 (0.7) (0.7).5 Bowel obstruction In-stay 3 (0.4) 2 (0.6) (1.4).18 Post-release 4 (0.5) 2 (0.6) Total 7 (0.9) 4 (1.4) (1.3) 0.64 Colitis In-stay 6 (0.8) 4 (1.2) (2.9) 0.57 Post-release 3 (0.4) Total 8 (1.1) 4 (1.2) (3.5) 0.1 Sepsis In-stay 11 (1.5) 3 (0.9) (1.4) 1 Post-release 0 2 (0.6) (0.7) 0.16 Total 11 (1.5) 5 (1.5) 1 3 (2.2) 0.47 ICU = intensive care unit; NGT = nasogastric tube; NPO = nothing by mouth; TPN = total parenteral nutrition. Multivariate analysis Using multivariate models correcting for any significant covariates, all initial findings were confirmed; after correction for age and comorbidities in linear regression, patients with adhesions still had significantly longer operation times (both P<0.001) and longer P 143
11 Chapter 10 hospitalizations (P=0.029 for all adhesions and P<0.001 for dense adhesions). Conversion rates and prolonged and resumed NPO status also had unchanged significance levels after binary logistic regression, which included a significant increase in odds of conversion in sense adhesions (odds ratio (OR)=5.15, P<0.001) and a significant increase in the odds of unexpected NPO status in overall adhesions (OR=1.75, P=0.037). Table 5 displays these results in further detail. Table 5. Multivariate regression between the presence of adhesions and dependent variables controlling for significant covariates All adhesions Dense adhesions Beta P-value Beta P-value Linear regression Surgery duration (age, Charlson) < <0.001 Stay duration (age, Charlson) <0.001 Odds ratio P-value Odds ratio P-value Logistic regression Conversion (none) <0.001 NPO complication (Charlson) NPO = Nil Per Os -nothing by mouth Comments The impact of postoperative adhesions on long-term outcomes has been widely studied. However, there are still questions about the implications for patients who are about to undergo abdominal surgery and are expected to have adhesions. Specific evidence for colon cancer patients is even sparser. Because colon cancer patients tend to be among the oldest groups of patients undergoing major abdominal surgery, they are expected to have a higher incidence of previous abdominal surgeries and a higher comorbidity burden. Our intent was to measure the impact of adhesions in the perioperative setting in a large population of surgically treated colon cancer patients. We did so by comparing outcomes and complication rates during surgery and up to 30 days postoperatively. We found that adhesions were more frequent in older patients and in patients with higher Charlson comorbidity and ASA scores. Our findings confirm what one intuitively thinks, which is that adhesiolysis drastically lengthens operation duration, adding 40 minutes on average to a surgery that has a mean duration of 2 hours, thereby lengthening an average colon cancer surgery by 33%. Adhesions 144
12 Impact of adhesions on surgery and recovery complicate minimally invasive resections by leading to a 2- to 3-fold increase of conversion rates. In terms of postoperative recovery, an extensive evaluation of all major postoperative complications revealed only increased odds of having a delayed postoperative bowel function. Patients with adhesions subsequently had a significantly longer hospital stay, with a doubling of this effect in patients with dense adhesions. The link between adhesions and longer operation times confirms earlier suggestions by Coleman et al. 10 and Beck et al., 11 whereas the increase in conversion rates reiterates several reports that described the finding in other abdominal surgeries No further differences in complication rates were identified. A longer stay without increased complication rates is an indication that patients with adhesions do not have longer hospitalizations because of complications during their recovery but rather because of delayed gastrointestinal function from adhesiolysis as supported by the finding of a higher incidence of prolonged or resumed NPO status. This finding confirms a previous report describing higher rates of parenteral nutrition use in patients with adhesion-related inadvertent enterotomy. 15 An important limitation of this type of study is that it carries the inherent burden of reporting bias. The data collected here is based on operation and discharge reports. Meanwhile, it is quite conceivable that individual surgeons have different considerations on whether to report adhesions and how to describe these. However, the subjective judgment of the individual surgeon is an inherent limitation of this type of retrospective research, and by including over 1000 patients, we attempted to contain this effect as much as realistically possible. Furthermore, the overwhelming majority of our operative notes are dictated by attending surgeons within 12 hours of the operation, which hopefully increases accuracy and decreases recall bias. It is also possible that surgical learning curves impacted outcomes particularly in laparoscopic procedures. However, our population spans a time period that starts many years after the introduction of laparoscopic colectomies for colon cancer at our center. Whether there was still bias related to the learning curve and dealing with adhesions laparoscopically is unknown but doubtful considering the level of experience of our surgeons with laparoscopic procedures at the start of this patient series in It has also already been reported that many complications are underreported in discharge reports. 16, 17 However, an important nuance to add is that this supposed underreporting will probably cause a reporting bias that would favor more detailed reporting of the most complex cases. This could actually make it more likely to find significantly higher 145
13 Chapter 10 complication rates in the adhesions group, especially because they have higher Charlson comorbidity and ASA scores. Despite finding this link between higher comorbidity scores and adhesions, complication rates did not significantly differ. Even with a possible underreporting of complication rates, our population remains large enough to draw reliable conclusions from our statistical outcomes. In other words, it allows us to show with a reasonable level of certainty that the impact of pre-existent adhesions on short-term postoperative complications is low. In conclusion, our findings prove that pre-existing adhesions increase the operative and postoperative burden by significantly lengthening the surgical procedure, by increasing conversion rates, and by extending stay duration by leading to delayed gastrointestinal motility. Conversely, we can also conclude that these pre-existing adhesions do not cause more complications in a patient's postoperative course in our colon cancer population. 146
14 Impact of adhesions on surgery and recovery References 1. Liakakos T, Thomakos N, Fine PM, Dervenis C, Young RL. Peritoneal adhesions: etiology, pathophysiology, and clinical significance. Recent advances in prevention and management. Dig Surg. 2001;18(4): Beck DE, Opelka FG, Bailey HR, Rauh SM, Pashos CL. Incidence of small-bowel obstruction and adhesiolysis after open colorectal and general surgery. Dis. Colon Rectum Feb;42(2): Meagher AP, Farouk R, Dozois RR, Kelly KA, Pemberton JH. J ileal pouch-anal anastomosis for chronic ulcerative colitis: complications and long-term outcome in 1310 patients. Br J Surg Jun;85(6): Barmparas G, Branco BC, Schnüriger B, Lam L, Inaba K, Demetriades D. The incidence and risk factors of post-laparotomy adhesive small bowel obstruction. J. Gastrointest. Surg Oct;14(10): Ehrenfeld JM, Seim AR, Berger DL, Sandberg WS. Implementation of a direct-fromrecovery-room discharge pathway: a process improvement effort. Surg Innov. 2009;16(3): Pandya S, Murray JJ, Coller JA, Rusin LC. Laparoscopic colectomy: indications for conversion to laparotomy. Arch Surg May;134(5): van Goor HH. Consequences and complications of peritoneal adhesions. Colorectal Dis Oct 1;9 Suppl 2: Binenbaum SJ, Goldfarb MA. Inadvertent enterotomy in minimally invasive abdominal surgery. JSLS Jul;10(3): Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5): Coleman MG, McLain AD, Moran BJ. Impact of previous surgery on time taken for incision and division of adhesions during laparotomy. Dis. Colon Rectum Sep;43(9): Beck DE, Ferguson MA, Opelka FG, Fleshman JW, Gervaz P, Wexner SD. Effect of previous surgery on abdominal opening time. Dis. Colon Rectum Dec;43(12): Schwartz ML, Drew RL, Chazin-Caldie M. Factors determining conversion from laparoscopic to open Roux-en-Y gastric bypass. Obes Surg Oct;14(9): Sokol AI, Chuang K, Milad MP. Risk factors for conversion to laparotomy during gynecologic laparoscopy. J Am Assoc Gynecol Laparosc Nov;10(4): Perrone JM, Soper NJ, Eagon JC, Klingensmith ME, Aft RL, Frisella MM, et al. Perioperative outcomes and complications of laparoscopic ventral hernia repair. Surgery Oct;138(4): discussion Van Der Krabben AA, Dijkstra FR, Nieuwenhuijzen M, Reijnen MM, Schaapveld M, van Goor H. Morbidity and mortality of inadvertent enterotomy during adhesiotomy. Br J Surg Apr;87(4): Bertges DJ, Shackford SR, Cloud AK, Stiles J, Stanley AC, Steinthorsson G, et al. Toward optimal recording of surgical complications: concurrent tracking compared to the discharge data set. Surgery Jan;141(1): Wanzel KR, Jamieson CG, Bohnen JM. Complications on a general surgery service: incidence and reporting. Can J Surg Apr;43(2):
The impact of adhesions on operations and postoperative recovery in colon cancer surgery
The American Journal of Surgery (2013) -, - - The impact of adhesions on operations and postoperative recovery in colon cancer surgery Ramzi Amri, M.Sc., Hannah C. den Boon, B.Sc., Liliana G. Bordeianou,
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