Surg Endosc DOI 10.1007/s00464-014-3814-1

and Other Interventional Techniques

Iatrogenic ureteral injury in colorectal cancer surgery: a nationwide study comparing laparoscopic and open approaches Peter Andersen • Lars Maagaard Andersen Lene H. Iversen



Received: 14 May 2014 / Accepted: 14 August 2014 Ó Springer Science+Business Media New York 2014

Abstract Background Iatrogenic ureteral injury is a rare complication in colorectal surgery. We aimed to investigate the risk of ureteral injury among patients with colorectal cancer operated on with curative intent in Denmark with laparoscopic and open technique. Method The study was based on the Danish National Colorectal Cancer database (DCCG) and included patients treated with intended curative resection for colorectal cancer between 2005 and 2011. From the DCCG database, we extracted data on intraoperative urinary tract injuries. To identify urinary tract injuries not recognized at the time of surgery but within 30 days after surgery, we crosslinked data with the National Patient Registry. All ureteral injuries were confirmed by medical record review. Data were analyzed separately for colon and rectal cancer. Results A total of 18,474 patients had a resection for colorectal cancer. Eighty-two ureteral injuries were related to colorectal surgery. The rate of ureteral injuries in the entire cohort was 0.44 %, with 37 (0.59 %) injuries in the laparoscopic group (n = 6,291) and 45 (0.37 %) injuries in the open group (n = 12,183), (P = 0.03). No difference in ureteral injury was found in relation to surgical approach in colon cancer patients. In rectum cancer patients (n = 5,959), the laparoscopic approach was used in 1,899

ON BEHALF OF DCCG. P. Andersen (&)  L. H. Iversen Department of Surgery P, Aarhus University Hospital, Tage-Hansens Gade 2, 8000 Aarhus C, Denmark e-mail: [email protected] L. M. Andersen Department of Surgery, Regional Hospital Randers, Randers, Denmark

patients, and 19 (1.00 %) had ureteral injuries, whereas 17 (0.42 %) of 4,060 patients who underwent an open resection had a ureteral injury. In multivariate analysis adjusted for age, gender, ASA score, BMI, tumor stage, preoperative chemo-radiation, calendar year, and specialty of the surgeon, the laparoscopic approach was associated with an increased risk of ureteral injury, OR = 2.67; 95 % CI 1.26–5.65. Conclusion In this nationwide study laparoscopic surgery for rectal cancer with curative intent was associated with a significantly increased risk of iatrogenic ureteral injury compared to open surgery. Keywords Colorectal surgery  Ureteral injury  Population-based  Minimal invasive  Surgical procedures  Laparotomy  Colorectal neoplasms

The first laparoscopic colonic resections were performed in the early 1990s [1]. Since then, the laparoscopic approach in colorectal surgery has been implemented to varying degrees worldwide. In Denmark, only 9.8 % [2] of the colorectal cancer resections were performed laparoscopically in 2005, increasing to 59.6 % in 2012 [3], and today it is the surgical standard treatment for colorectal cancer patients in Denmark. Several studies have compared outcome in laparoscopic and open colectomy and found no differences in morbidity, mortality, positive resection margins, and number of identified lymph nodes. Laparoscopic colectomy is associated with earlier recovery of bowel function, reduced need for analgesics, and a shorter hospital stay. However, the surgical operating time is significantly longer [4–10]. Implementation of laparoscopic surgery into some new areas may in some instances temporarily increase the

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incidence of iatrogenic injuries. For instance, when laparoscopic cholecystectomy was introduced, the rate of biliary duct injury increased. With time, the bile-duct injury rate decreased to a level comparable with that of open cholecystectomy [11–13]. In laparoscopic hysterectomy, an increased risk of iatrogenic urinary tract injuries has been observed in comparison with abdominal hysterectomy [14]. Iatrogenic ureteral injury is a serious, but rare complication associated with increased morbidity [15–17]. Although surgeons always pay great attention to the ureters during colorectal surgery, the incidence of ureteral injury in laparoscopic colorectal surgery compared with open surgery has only been sparingly evaluated. An increased risk of iatrogenic ureteral injury in laparoscopic colectomy has been shown in a single study. The study included 5,729 patients treated for benign as well as malignant colorectal diseases and found a significantly increased incidence of iatrogenic ureteral injury after laparoscopic versus open colectomy (0.66 vs 0.15 %, P = 0.007) [16]. In contrast, a recent nationwide study from the United States including 6,027 iatrogenic ureteral injuries has shown that laparoscopic approach was not associated with iatrogenic ureteral injury in colorectal surgery [17]. Patients were treated for benign as well as malignant colorectal diseases, and the indication for and frequency of the laparoscopic approach was not given. The aim of the present study was to investigate the risk of iatrogenic ureteral injury in laparoscopic and open surgery for colorectal cancer among patients operated on with curative intent in Denmark during the period of 2005–2011.

Materials and methods The study included patients who had an intended curative colon or rectal cancer resection during the period of January 1st 2005 to 31st of December 2011 and were registered in the Danish Colorectal Cancer Group’s (DCCG) database. Data sources The DCCG database is a national database that includes prospectively registered patients with a first time diagnosis of colorectal adenocarcinoma in Denmark. The database has existed since May 2001, and the patient completeness rate is over 96 % [3]. Patients are identified by a unique civil registry number, which has been given to every Danish resident since 1968. The database contains information on patient characteristics, stage of disease, operative data, intra- and postoperative complications within 30 days after surgery, and treatment. Data are reported by surgeons.

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From the DCCG database, we identified the study population and extracted data on intraoperative iatrogenic urinary tract injuries. Urinary tract injury registered in the DCCG database included ureteral injury, bladder injury, and urethral injury. To ensure that we identified all potential injuries, we also included patients who had a ureteral resection registered. To identify iatrogenic urinary tract injuries not recognized intraoperativley, but within 30 days after surgery, we cross-linked DCCGs data with the National Patient Registry (NPR). The NPR was established in 1977 and is used to collect data from all hospital admissions. Data include civil registry number, dates of admission and discharge, surgical procedure(s), and discharge diagnosis. We used the International Classification of Disease (ICD-10) codes and surgical treatment codes according to the Nordic Classification of Surgical Procedures (NCSP) [18] for diagnosis and procedures (DT812, DT812A, DT812B, DT812U, DT812UC, DS371, DT149, DT812V, DT812W, KKBH00, KKBH01, KKBH06, KKBH10, KKBH20, KKBH21, KKBH40, KKBV00, KKBV01, KKBV02, KKBV02A, KKBV05, KKBV10, KKBV12, KKBW96, KKAJ00, KKAJ97, KKBA96) related to urinary tract injury. Ureteral injury We reviewed medical records of all patients who, based on the DCCG database or the NPR, had a potential ureteral injury. Only ureteral injuries confirmed by intraoperative identification, postoperative radiographic imaging, and/or determination of significantly increased levels of creatinine in drainage liquid were included in the analysis. One surgical resident reviewed all medical records (PA), and if in doubt whether a potential injury could be confirmed or not, consensus was obtained between PA and a consultant surgeon (LMA). We categorized the confirmed injuries into ureteral injuries occurred during open surgery or laparoscopic surgery. If laparoscopic surgery was converted to open surgery, we categorized the ureteral injury according to the part of the operation during which it occurred. The site and location of ureteral injury as well as management of the injuries were registered from the medical records. We defined a distal ureteral injury as an injury situated distal to the common iliac artery. The study was approved by Danish data protection agency (record number 2012-41-0416). Statistical analysis Continuous data were transformed into categorical variables and presented as numbers and percentages. Differences in variables among patients operated on using a

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laparoscopic technique were compared with those in whom an open technique was used by means of the Chi-square test or Fischer’s exact test. Logistic regression analysis, adjusting for gender, age, ASA score, body mass index (BMI), T stage, tumor site, preoperative (chemo)-radiotherapy, year of surgery, and specialty of surgeon, was performed to evaluate the independent role of the surgical approach on ureteral injury. Results were presented as odds ratios (OR) and their 95 % confidence intervals (CI). Analyses were not only performed for all patients, but also for patients with colon and rectum cancer separately. Analyses were considered statistically significant if P \ 0.05. Statistical analyses were carried out using IBM SPSS Statistics for Windows, Version 19.0. Armonk, NY: IBM Corp.

Results A total of 18,474 patients underwent intended curative resection for colorectal cancer in Denmark from 2005 through 2011. Patient characteristics are listed in Table 1. Open surgery was performed in 12,183 (66.0 %) patients, and 6,291 (34.0 %) patients underwent laparoscopic surgery. The two groups according to surgical approach were comparable with respect to gender, but patients operated on laparoscopically were younger, had a lower ASA grade, a lower BMI, a less advanced tumor stage, and accordingly, fewer had received preoperative chemo-radiation. Tumors approached laparoscopically were more often located in the colon, and surgeons were more often colorectal specialist. The skewed distribution of the above-mentioned factors among patients operated on by laparoscopic and open techniques was also observed when colon cancer patients were analyzed separately, and the same was true in rectal cancer patients, but with two exceptions: comparable age distribution, but more women were operated on laparoscopically. We found 245 potential iatrogenic urinary tract injuries by combining the DCCG and NPR registries. On medical record review, we found that 131 patients had other iatrogenic urinary tract injuries than ureteral injury. We excluded 32 ureteral injuries for a variety of reasons (Fig. 1). Sixteen patients had tumor growth into the ureter. Nine patients had an intended resection of the ureter. Four ureteral injuries occurred in a gynecological part procedure conducted by a gynecologist. In two patients, it was unclear whether the ureteral injury occurred during the laparoscopic or open part of the surgery, and finally, one patient had a ureteral injury due to prophylactic placement of a ureteral stent. Thus, a total of 82 ureteral injuries were included in the analysis.

Table 1 Characteristics of patients undergoing intended curative surgery for colorectal cancer in Denmark, 2005–2011, n = 18,474 Open resection No. of patients (%)

Laparoscopic resection No. of patients (%)

12,183 (66.0)

6,291 (34.0)

Male

6,448 (52.9)

3,272 (52.0)

Female

5,735 (47.1)

3,019 (48.0)

3,559 (29.2)

1,951 (31.0)

Total Gender

0.244

Age (years) \65

P value

0.006

65–75

4,435 (36.4)

2,312 (36.8)

[75

4,189 (34.4)

2,028 (32.2) \0.001

ASA grade I–II III

9,001 (73.9) 2,706 (22.2)

5,178 (82.3) 995 (15.8)

IV–V

221 (1.8)

48 (0.8)

Missing

225 (2.1)

70 (1.1) \0.001

Body mass index (kg/m2) \20

773 (6.3)

356 (5.7)

20–29

6,794 (55.8)

3,999 (63.6)

C30

1,386 (11.4)

724 (11.5)

Missing

3,230 (26.5)

1,212 (19.3)

I

1,674 (13.7)

1,385 (22.0)

II III

4,926 (40.4) 4,018 (33.0)

2,366 (37.6) 1,969 (31.3)

IV

1,459 (12.0)

513 (8,2)

Missing

106 (0.9)

58 (0.9)

Colon

8,123 (66.7)

4,392 (69.8)

Rectum

4,060 (33.3)

1,899 (30.2)

\0.001

T stage

\0.001

Tumor site

\0.001

Preoperative (chemo)radiation No

10,779 (88.5)

5,799 (92.2)

Yes

1,404 (11.5)

492 (7.8)

2005 2006

2,199 (18.0) 2,163 (17.8)

266 (4.2) 535 (8.5)

2007

1,959 (16.1)

680 (10.8)

2008

1,718 (14.1)

902 (14.3)

2009

1,405 (11.5)

1,229 (19.5)

2010

1,487 (12.2)

1,253 (19.9)

2011

1,252 (10.3)

1,426 (22.7)

Colorectal

1,896 (15.6)

1,953 (31.0)

Gastrointestinal

7,402 (60.8)

3,722 (59.2)

General/not specialist

2,885 (23.7)

616 (9.8)

\0.001

Year of surgery

\0.001

Specialty of surgeon

Using v2 test or Fischer’s exact test

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Surg Endosc Fig. 1 Flow chart of patients with potential ureteral injury included in the study

Table 2 Risk of ureteral injury at colorectal cancer resection according to surgical approach Odds ratio (95 % CI) Surgical approach

P value 0.042

Open

1.00 (ref)

Laparoscopic

1.64 (1.02–2.63)

Adjusted for age, gender, ASA score, body mass index, T stage, tumor site, preoperative (chemo-)radiation, calendar year, and specialty of surgeon

The rate of iatrogenic ureteral injuries in the entire cohort (18,474) recognized within 30 days of surgery was 0.44 %. Ureteral injury occurred among 37 (0.59 %) in the laparoscopic surgery group and 45 (0.37 %) in the open surgery group (P = 0.03). In multivariate analysis adjusting for age, gender, ASA score, BMI, tumor stage and -site, preoperative chemoradiation, calendar year, and specialization of surgeon, laparoscopic approach was significantly associated with an increased risk of iatrogenic ureteral injury, OR = 1.64; 95 % CI 1.02–2.63 (P = 0.04), Table 2. In analyses stratified for tumor site, we found 12,515 patients who had an intended curative resection for colon cancer. Laparoscopic surgery was performed in 4,392 patients, among whom 18 (0.41 %) patients had a ureteral injury. An open approach was used in 8,123 patients, which resulted in 28 (0.34 %) ureteral injuries. The rate of

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ureteral injury did not differ significantly according to surgical approach, P = 0.34. In rectal cancer patients, a total of 5,959 patients underwent intended curative resections, among whom 1,899 patients had a laparoscopic approach, and 19 (1.00 %) patients had ureteral injuries, whereas 4,060 patients underwent open resection, which resulted in 17 (0.42 %) ureteral injuries, P = 0.007. In multivariate analysis adjusted for age, gender, ASA score, BMI, tumor stage, preoperative chemo-radiation, calendar year, and specialization of surgeon, the laparoscopic approach was associated with a significantly higher risk of iatrogenic ureteral injury, OR = 2.67; 95 % CI 1.26–5.65 (P = 0.010) compared with open surgery. The majority of ureteral injuries were recognized intraoperatively irrespective of surgical approach, Table 3. Median time to diagnosis of ureteral injury not recognized intraoperatively was 13.5 days (range 5–29 days) in the open group versus 9.4 days (range 4–16 days) in the laparoscopic group. The most frequent diagnostic modality used in injuries recognized after surgery was computed tomography (CT) urography, Table 3. Pyelography and determination of creatinine in drainage liquid were also used. Ureteral injuries occurred more frequently to the left ureter, 27 (73.0 %), in the laparoscopic group than in the open surgery group 21 (47.7 %), P = 0.024. The most frequent location of injuries was the distal ureter irrespective of surgical approach. Missing data for location of

Surg Endosc Table 3 Timing of diagnosis, diagnostic modality, location of ureteral injury, and management of ureteral injury Open resection No. of patients (%) Ureteral injury (UI)

Laparoscopic resection No. of patients (%)

45

37

Intraoperatively

32 (71.1)

27 (73.0)

Postoperatively

13 (28.9)

10 (27.0)

CT urography

7

6

Pyelography

2

1

Creatinine in drainage

4

3

24 (53.3) 21 (47.7)

10 (27.0) 27 (73.0)

Proximal UI

6 (13.3)

6 (16.2)

Distal UI

18 (40.0)

15 (40.5)

Missing

21 (46.7)

16 (43.2)

Timing of diagnosis

Diagnostic modality

Site of UI Right ureter Left ureter Location of UI

Treatment of UI Ureteroureterostomy

29 (64.4)

21 (56.8)

Nephrostomy

8 (17.8)

7 (18.9)

Ureteroneocystostomy

4 (8.9)

5 (13.5)

Ureteral stent

4 (8.9)

4 (10.8)

ureteral injury was high due to poor description by the surgeons of ureteral injury recognized intraoperatively.

Discussion This nationwide study has shown an iatrogenic ureteral injury rate of 0.44 % after intended curative colorectal cancer resection in Denmark. The laparoscopic approach in colorectal cancer surgery was associated with a 1.6-fold increase of iatrogenic ureteral injury as compared with open surgery. In rectal cancer surgery, the risk of ureteral injury was even higher, with a 2.7-fold (95 % CI 1.3–5.7) increase, when a laparoscopic technique was used. Consistent with our findings, a retrospective study from a single center of 5,729 patients with 14 ureteral injuries after colectomies performed for benign as well as malignant diseases showed a significant increase of iatrogenic ureteral injury occurring after laparoscopic surgery (n = 1,060) compared with open surgery (n = 4,669), 0.66 versus 0.15 %, P = 0.007 [16]. In contrast, in a recent nationwide retrospective study from the United States, use of the laparoscopic approach appeared to be a protective factor of iatrogenic ureteral injuries in colorectal surgery

[17]. The study described 6,027 iatrogenic ureteral injuries among an estimated number of surgeries for benign and malignant diseases, but no information on whether laparoscopic surgery was performed to the same degree in benign and malignant conditions. Interestingly, a high rate of ureteral injuries in laparoscopic operations converted to open surgery was found, but there was no mention of whether iatrogenic ureteral injury was a contributing factor for conversion of the operation. When laparoscopic and converted operations were analyzed together, no differences were observed between the rates of ureteral injury after laparoscopic and open surgery. In a predictive model for ureteral injury, the authors found rectal cancer to be a risk factor for ureteral injury. The latter observation is in accordance with our results. Several studies have demonstrated an increased incidence of iatrogenic urinary tract injury in laparoscopic hysterectomy. A Cochrane review [14] that included randomized controlled trials on the surgical approach in hysterectomy for benign gynecological disease showed a 2.7fold (95 % CI 1.31–5.63) increased risk of urinary tract injury for laparoscopic hysterectomy versus open hysterectomy. Bladder and ureteral injuries were pooled as urinary tract injury. A learning curve phenomenon has been suggested as a possible explanation for the higher incidence of urinary tract injuries in laparoscopic hysterectomy [19, 20]. Our study was performed during an implementation period for laparoscopic colorectal surgery in all of Denmark. Only continuous audit of the national data will reveal, whether the increased risk of iatrogenic ureteral injury in laparoscopic colorectal cancer surgery is due to a learning curve phenomenon. Furthermore, other nationwide studies are needed to confirm our results. Interestingly, we found a significant left-sided predominance of ureteral injuries, 75 %, in the laparoscopic group compared to no difference with regard to side of injury in the open group: a finding, which to our knowledge, has not been reported previously. This left-sided predominance of ureteral injuries may be due to the medial to lateral approach [21] commonly used in laparoscopic colorectal surgery. If the medial to lateral dissection has not been completed far enough laterally, the ureter may be injured when dividing Toldt’s fascia laterally. Another possible risk may be if the surgeon goes to deeply into the retroperitoneum and thereby below the ureter when identifying the plane between the mesocolon and the retroperitoneum. Especially in very thin patients, surgeons may dissect too deeply and inadvertently invade the retroperitoneum. This finding underlines the importance of a correct dissection plane, and, if in doubt, the surgeon should identify the ureter. Three-quarters of iatrogenic ureteral injuries were recognized intraoperatively both in the laparoscopic and in the

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open group. It has been reported that iatrogenic ureteral injuries in laparoscopic surgery are less frequently discovered intraoperatively compared with open surgery [22]. Our study does not confirm this observation. The timing of diagnosis of iatrogenic ureteral injury has been reported over a wide range. In the colorectal study on 14 ureteral injuries by Palaniappa, half of the ureteral injuries were recognized intraoperatively [16]. In open colectomy, it has been reported that 60 % of ureteral injuries were recognized intraoperatively [23]. In a study analyzing iatrogenic ureteral injury in urological, obstetrics/gynecological and general surgery combined, 68.3 % of iatrogenic ureteral injuries were recognized intraoperatively [15]. Our rate of intraoperatively recognized ureteral injury was even higher. The literature examining when postoperative iatrogenic ureteral injury was recognized is conflicting. Some have recognized iatrogenic ureteral injury later than 30 days postoperatively [15, 22, 23], and others have not recognized any injuries later than 30 days postoperatively [24, 25]. The latest postoperatively recognized iatrogenic ureteral injury in our study was 29 days. This finding underlines the importance of having at least 30 days’ follow-up in order not to underestimate iatrogenic ureteral injury. The majority of iatrogenic ureteral injuries occurred in the distal part of the ureter in both groups. However, this observation should be interpreted with caution, because data were missing in a high proportion of patients. Surgeons’ descriptions of the localization of ureteral injuries recognized intraoperatively were insufficient. Other studies have reported that op till 90 % of iatrogenic ureteral injuries were located in the distal part of ureter [22, 23]. The preoperative placement of lighted ureteral stents has been suggested as a way to protect the ureters, but the procedure remains controversial because the risk of injury during initial placement is reported to be 1.1 % [26, 27] In addition, there is an increased risk of urinary tract infection after placement of ureteral stents [28]. Given the low incidence of iatrogenic ureteral injuries, it is an additional time-consuming procedure with potential morbidity. It is not required in general, but the use of prophylactic ureteral stents could be considered in special cases such as advanced tumors adjacent to the ureter. Injection of intravenous indigo carmine dye, which colors the urine blue, followed by cystoscopy to ensure patency of the ureters after laparoscopic hysterectomy [24, 29] has been suggested because the dye makes it easier to identify a urinary tract injury. To our knowledge a similar trial has never been performed in colorectal surgery, and it is doubtful whether use of this dye could play a role in laparoscopic colorectal surgery. The use of a robotic approach has been suggested to provide an advantage during pelvic dissection [30]. The

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implementation of robotic approach could, perhaps, decrease the incidence of iatrogenic ureteral injury in rectal cancer surgery, but this has yet to be investigated. Duplicated ureter is a congenital condition occurring in approximately 1 % of the population [31]. The presence of this condition could increase the risk of iatrogenic ureteral injury because the surgeon might injure the duplicated ureter, while thinking the identification had already been completed. However, this risk must be independent of surgical approach. The main strengths of this study include its nationwide population, the size of the cohort, and the prospective registration to the DCCG database, with its high validity and accuracy of data. All iatrogenic ureteral injuries were confirmed by medical record review, and we had a 30-day follow-up period from the NPR. Limitations of our study include the missing information on surgeons’ experience. Furthermore, we do not have an explanation as to why patients were selected for laparoscopic or for open surgery was different, but it reflects daily clinical practice. Patients chosen for laparoscopic surgery during the implementation period in Denmark were potentially less complicated patients to operate (lower BMI and T stage), and they were more frequently operated on by surgeons sub-specialized in colorectal surgery. Our results were, however, adjusted for these factors. It has been hypothesized that operating on an irradiated pelvis is challenging along with the ureters adjacent to the dissection plane may lead to higher rates of iatrogenic ureteral injuries [17]. Nevertheless, we observed a higher rate of iatrogenic ureteral injuries in patients in whom a laparoscopic approach in rectal cancer surgery was used. In conclusion, in this study laparoscopic surgery compared to open surgery for rectal cancer with curative intent was associated with a significantly increased risk of iatrogenic ureteral injury. However, other nationwide studies are warranted to confirm our results. Acknowledgments The Danish Colorectal Cancer Group is thanked for Granting access to the database. Dr. Steffen Høgskilde provided technical assistance by extracting data from the DCCG database and the National Patient Registry. Statistical analysis was done in cooperation with Leif Spange Mortensen, M.Sc. Disclosures Drs. Peter Andersen, Lars Maagaard Andersen, and Lene H. Iversen have no conflict of interest or financial ties to disclose. Funding Lene Iversen was supported by Grants from the Danish Council for Independent Research/Medical Sciences (10-081843).

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Iatrogenic ureteral injury in colorectal cancer surgery: a nationwide study comparing laparoscopic and open approaches.

Iatrogenic ureteral injury is a rare complication in colorectal surgery. We aimed to investigate the risk of ureteral injury among patients with color...
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