- Email: [email protected]
Laparoscopic surgery for radiation enteritis
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Laparoscopic surgery for radiation enteritis Jian Wang, MD, PhD, Danhua Yao, MD, PhD, Shaoyi Zhang, MD, Qi Mao, MD, PhD, Yousheng Li, MD, PhD,* and Jieshou Li, MD, PhD Department of Surgery, Jinling Hospital, Nanjing University School of Medicine, Nanjing, China
article info
abstract
Article history:
Background: The aim of this study was to determine the safety and feasibility of laparo-
Received 29 August 2014
scopic surgery for radiation enteritis-induced intestinal stenosis requiring ileocecal
Received in revised form
resection.
30 October 2014
Methods: Clinical records of radiation enteritis patients that underwent laparoscopic ileo-
Accepted 14 November 2014
cecal resection and ileo-ascending colonic side-to-side anastomosis in a single center from
Available online 21 November 2014
January 2012eFebruary 2014 were retrospectively analyzed. Thirty patients were identified and matched by abdominal adhesion grade, age, gender, primary malignancy distribution,
Keywords:
previous abdominal surgery history, and body mass index to 30 patients that underwent
Laparoscopic surgery
open surgery for the same procedure from August 2009eDecember 2011. General infor-
Radiation enteritis
mation, operative findings, and short-term outcomes were compared between the two
Case-matched study
groups. Results: The conversion rate of laparoscopic surgery was 23.3%. The length of skin incision in the laparoscopic group was significantly shorter than that of the open surgery group (6.8 cm versus 15.8 cm, P ¼ 0.001). Laparoscopic surgery significantly decreased recovery time to total enteral nutrition (10.3 d versus 15.6 d, P ¼ 0.037); however, postoperative hospital stay was not significantly different between the two groups (28.2 d versus 32.4 d, P ¼ 0.924). Intraoperative blood loss (125 mL versus 189 mL, P ¼ 0.000) and operation time (138 min versus 171 min, P ¼ 0.003) were significantly improved in the laparoscopic group compared with those in the open surgery group. Laparoscopic surgery did not significantly decrease postoperative morbidity but did decrease the pleural effusion rate. Conclusions: Laparoscopic surgery is feasible for treatment of radiation enteritis-induced intestinal stenosis with a relatively low conversion rate. Laparoscopic surgery is as safe as open surgery and is superior to open surgery with decreased skin incision length, operation time, intraoperative blood loss, and postoperative recovery time to total enteral nutrition. ª 2015 Elsevier Inc. All rights reserved.
1.
Introduction
Radiation enteritis (RE) is an intestinal damage, represented by a spectrum of clinical manifestations, caused by abdominal or pelvic radiation. Surgical treatment is necessary for intestinal stenosis, intestinal perforation, and occasionally,
gastrointestinal hemorrhage [1]. Three to fifteen percent of RE patients will develop radiation enteritis-induced intestinal stenosis (REIIS) [2]. For REIIS, the surgical challenge lies in the dense intra-abdominal adhesion and fibrosis [3]. Postoperative complications including wound or anastomosis healing complications remain obstacles in traditional open
* Corresponding author. Department of Surgery, Jinling Hospital, Nanjing University School of Medicine, 305 East Zhongshan Road, Nanjing 210002, China. Tel.: þ86 25 8086 0137; fax: þ86 25 8541 9980. E-mail address: [email protected] (Y. Li). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2014.11.026
416
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
surgery [4]. The development of laparoscopic surgery has expanded the use of this technique from cholecystectomy to gastrointestinal cancer, and to other complicated inflammatory diseases such as Crohn disease [5] with the advantages of this technique simultaneously being identified. From 2012, the authors began to perform laparoscopic surgery for cases of RE. The aim of this study was to summarize the preliminary experience of laparoscopic surgery for REIIS and to determine the safety and feasibility of this technique.
2.
Materials and methods
2.1.
Patients
Laparoscopic surgery was introduced in our center on January 2012 by a team of surgeons. Clinical records of RE patients that presented with ileum stenosis and that underwent laparoscopic ileocecal resection and ileo-ascending colonic side-toside anastomosis from January 2012eFebruary 2014 were retrospectively reviewed. Patients that underwent open surgery for the same procedure in an earlier era, August 2009eDecember 2011 by the same unique team of surgeons, were 1:1 matched in terms of abdominal adhesion grade, age, gender, primary malignancy distribution, total radiation dose, interval between radiation and surgery, previous abdominal surgery history, and body mass index (BMI). All patients with REIIS in the two periods were considered for inclusion in this study. The exclusion criteria included emergent surgery, malignancy recurrence, preoperative short bowel syndrome (remnant small intestine <150 cm), or intraperitoneal chemotherapy history. The diagnosis was determined by clinical history, computed tomography (CT) manifestation, and confirmed by intraoperative and histologic findings. All patients presented with fibrosis and stenosis with the final 20 cm of the ileum affected. This was the pathologic basis of ileocecal resection [4]. All patients underwent preoperative parenteral or enteral nutritional support if they suffered malnutrition, as confirmed by low serum albumin levels. Operative findings and short-term outcomes were compared between the two groups including intraoperative blood loss; operation time; length and site of skin incision; conversion rate to open surgery; postoperative morbidity rate; recovery time to total enteral nutrition (TEN); and postoperative hospital stay. All surgical treatments were performed with informed signed consent, and the study was approved by the Medical Ethics Committee of Nanjing University.
2.2.
Operative techniques
For the laparoscopic group, when performing the dissection, a total laparoscopic technique was adopted. For all cases, four to five laparoscopic ports (5e12 mm in diameter) were used. A 12-mm supraumbilical port was used for the laparoscope and camera. The working ports included one 5-mm port placed in the right upper quadrant, one 5e12-mm port placed in the left upper quadrant, and a 12-mm trocar placed in the right iliac fossa. An additional 5-mm trocar was placed in the left iliac fossa if necessary. The ports were integrally moved 5 cm upward to be distant from previous incisions, if the previous
incisions expanded upward toward the navel. The first port was routinely made via the open method. Mobilization and dissection under a laparoscope was achieved using ultrasonic scissors (Ethicon Surgical Care, Somerville, NJ). After the exclusion of malignancy recurrence, the ileocecal and distal ileum were mobilized from the pelvic cavity, and blood supply of the lesion was discontinued by ultrasonic scissors or clips. After resection of the lesion, stapled ileo-ascending colonic side-to-side anastomosis was performed using staples (Ethicon Surgical Care) inside the abdomen or outside the abdomen with an adjuvant incision, which is in general on the upper abdomen for removing the intestinal lesion. Intraoperative bleeding was controlled by the use of metal clips or ultrasonic scissors. For open surgery, a lower-abdominal vertical or transverse incision was made for abdominal exposure. Dissection and anastomosis in these cases followed the same techniques as the laparoscopic surgery mentioned previously.
2.3.
Adhesion grading system
An intraperitoneal adhesion grading system specific to RE was initiated. The adhesion was divided into five grades as shown in Table 1. It should be noted that all adhesions discussed here are limited to adhesions between the intestines and the abdominal wall, pelvic wall, or pelvic contents. Adhesions among the intestinal lesions are not included as these cases required resection en bloc rather than lysis.
2.4.
Postoperative care
Parenteral nutrition was initiated on postoperative days 2e3. Simultaneously, enteral nutrition was administered through a nasogastric tube or gastrostoma. Parenteral nutrition was discontinued when enteral nutrition was achieved to full strength (25 kcal/kg/d). Postoperative complications were treated accordingly.
2.5.
Statistics
Results are presented as median (range) for quantitative outcomes and as frequencies for categorical outcomes. All outcomes were compared between the open surgery group and the laparoscopic surgery group. ManneWhitney tests for unpaired data were used for comparisons of age, total radiation
Table 1 e Adhesion grading system. Grade 0 1 2 3 4
Description No adhesion between the affected intestinal lesions and surrounding organs Adhesion and fibrosis limited to right pelvis Strong adhesion and fibrosis affecting whole pelvis, organs strongly attached with severe adhesions Grade 2 adhesion extending between intestine and anterior pelvic wall Grade 3 adhesion extending between intestine and anterior abdominal wall
417
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
Table 2 e General information of the patients. General information
Open surgery (n ¼ 30)
Laparoscopic surgery (n ¼ 30)
P value
52.1 (34e68) 2: 28
52.9 (34e71) 3: 27
0.761 1.000 0.844
18 6 5 1 52.9 (44e66) 34.8 (6e290) 27 19.9 (14.0e26.9)
17 4 6 3 51.2 (30e70) 32.4 (6e176) 30 19.0 (13.0e24.1)
Mean age (range, y) Gender (male: female) Primary malignancy Cervical carcinoma Endometrial cancer Rectal cancer Others Total radiation dose (Gy) Interval between radiation and surgery (mo) Number of patients with previous abdominal operations BMI (kg/cm2)
dose, interval between radiation and surgery, BMI, blood loss, operation time, length of skin incision, recovery time to TEN, and postoperative hospital stay. Chi-square tests were used for comparison of gender distribution, primary tumor distribution, previous abdominal surgery history, adhesion grade distribution, incision site distribution, and morbidity rate. All results were generated using SPSS statistical software (SPSS Inc, Chicago, IL). All tests were two-tailed, and P values of <0.05 were considered statistically significant.
3.
Results
Thirty patients were enrolled in the laparoscopic group and thirty patients were matched in the open surgery group. The groups were comparable for all matched factors including age; gender; primary malignancy distribution; previous abdominal surgery history; and BMI (Table 2). Abdominal adhesion grade was equivalent between the two groups (Table 3). Five intraoperative injuries occurred including two bladder injuries, two sigmoid colon injuries, and one external iliac artery injury (Table 4). All bladder injuries were successfully
repaired laparoscopically or under converted surgery during the operation without causing any postoperative complications. Sigmoid colon injuries were treated with preventative ileostomy. There was no significant difference between the two groups in terms of intraoperative injuries. Seven patients in the laparoscopic surgery group underwent conversion surgery. This was due to dense adhesion in four cases (grade 4 in three cases and grade 3 in one case), bladder injury in one case (grade 3), sigmoid colon injury in one case (grade 3), and external iliac artery injury in the final case (grade 1). Intraoperative blood loss and operation time were significantly lower in the laparoscopic group compared with those in the open surgery group. The skin incision length of the laparoscopic group was significantly shorter than that of the open surgery group (Table 3). In the 23 patients that underwent total laparoscopic surgery, 21 patients received a small right
Table 4 e Intraoperative injuries, postoperative morbidity, and short-term outcomes. Intra- and post-operative outcomes
Table 3 e Operative findings and results. Findings and results Adhesion grade 1 2 3 4 Intraoperative blood loss (mL) Operation time (min) Length of skin incision (cm) Incision Lower abdomen Upper abdomen Conversion rate NA ¼ not applicable.
Open surgery (n ¼ 30)
Laparoscopic surgery (n ¼ 30)
P value
7 12 9 2 189 (70e350)
10 6 11 3 125 (20e300)
0.000
171 (105e240)
138 (50e265)
0.003
15.8 (10e25)
6.8 (3e25)
0.001
30 0 NA
9 21 23.3%
0.403
0.000
NA
0.635 0.745 0.237 0.297
Intraoperative injuries Bladder Sigmoid colon External iliac artery Postoperative complications Incision infection or dehiscence Anastomotic leakage or fistula Pleural effusion Catheter Infection Cholestasis Abdominal bleeding Acute renal failure Recovery to TEN (postoperative day)* Postoperative hospital stay (d)* *
Open surgery Laparoscopic P value (n ¼ 30) surgery (n ¼ 30) 1 0 1 0 14
4 2 1 1 12
0.353 0.492 1.000 1.000 0.602
6
6
1.000
7
4
0.317
8 2 1 1 1 15.6 (4e61)
1 4 1 1 0 10.3 (4e22)
0.026 0.671 1.000 1.000 1.000 0.037
32.4 (13e111)
28.2 (12e56)
0.924
Patients with postoperative short bowel syndrome or ileostomy were not included.
418
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
Figure e Abdominal image from a patient who accepted a total laparoscopic procedure 6 mo ago. The lowerabdominal incision from a Dixon procedure performed 48 mo earlier failed to completely heal (white arrow), whereas the upper-right abdominal incision in laparoscopic surgery healed well (black arrow). (Color version of figure is available online.)
upper-abdominal incision (3e6 cm) and the remaining two patients received a right lower-abdominal incision that was previously an ileum stoma. No additional incision was made in these two patients. A total of 37 patients, including all patients in the open surgery group and the 7 patients that underwent conversed surgery in the laparoscopic group, received a lower-abdominal incision, with 19 patients receiving a transverse (10e20 cm) and 18 patients receiving vertical (8e25 cm) incisions. The general incision complication rate is presented in Table 4. A total of 11 of the 12 complications occurred in the lower-abdominal incisions, including 6 patients in the open surgery group, 4 patients that underwent conversed surgery, and 1 patient that underwent laparoscopic surgery. Only one incision complication occurred in an upper-abdominal incision. Figure is a representative image of a laparoscopic group case. The lower incision visible in the image was from a Dixon procedure conducted 48 mo earlier that failed to completely heal 6 mo after laparoscopic surgery, whereas the upper-abdominal incision from laparoscopic surgery healed well. Except for pleural effusion, there was no significant difference between the two groups in postoperative complications. Laparoscopic surgery significantly shortened the recovery time to TEN but did no decrease postoperative hospital stay (Table 4).
4.
Discussion
The short-term superiority of laparoscopic surgery has been well reported in routine gastrointestinal operation such as gastric or rectal cancer [6,7]. It is likely that this technique may also be advantageous in cases with more specific pathology,
such as RE. The intrinsic advantages of laparoscopic surgery (limited trauma, stress, and skin incision) make this procedure potentially beneficial to this group of patients that are generally characterized by malnutrition [8], incision complications, and uncertainty of malignancy recurrence. Although abdominal incisional complications are not as well defined as perineal wound after proctectomy, these complications remain the most common morbidity after radiation [9e11]. This is primarily due to abdominal wall damage as a result of the radiation [12]. In addition, wound length is a risk factor for wound infection in these patients [13]. Laparoscopic surgery can significantly shorten the incision length and can prevent the inclusion of the incision in the radiation field, which is generally conducted in the lower abdomen. This surgical strategy is promising to ultimately solve this incision problem. The data of the present study showed a significantly shorter incision length in the laparoscopic group; however, there was no significant difference in the rate of incision complications. There are four explanations for this inconsistency. First, the laparoscopic group included patients that underwent conversion surgery that resulted in four wound infections. Second, the laparoscopic group included one patient that failed to receive an incision in the healthy upper-abdominal wall. Third, the transverse incision was commonly used (17/30) in the open surgery group. Transverse incisions can partly move the incision away from the radiation field thereby possibly decreasing incision complications [14]. Finally, the sample size was relatively small, thus limiting interpretations of the data. The present study showed optimal results in operation time and intraoperative blood loss in the laparoscopic group. There was a significant decline in laparoscopic surgery operation time as cases growing (a decrease in time from 161 min for the first 15 procedures to 114 min for the second 15 procedures). The advantage of laparoscopic surgery in decreasing operation time is two-fold. First, pelvis exposure is improved in this technique allowing sharp, quick dissection and decreased blood loss. Second, the shortened incision in laparoscopic surgery significantly saves the time of abdominal closure. Laparoscopic surgery significantly decreased the rate of postoperative pleural effusion. Various factors are involved in the pathogenesis of nonspecific postoperative pleural effusion, including atelectasis, heart failure, transfusions during surgery, preoperative ascites, and hypoproteinemia, and so forth [15]. Few studies have compared the effect of laparoscopic surgery on postoperative pleural effusion. In one report, comparing the postoperative outcome between laparoscopic and open splenectomy and esophagogastric devascularization for bleeding varices or severe hypersplenism, lower pleural effusion was also found in the laparoscopic group [16]. In this article, the authors explained this result by improved postoperative physical activity in the laparoscopic group. In the present study, decreased skin incision length and pain may have also contributed to this improvement in postoperative outcomes. Laparoscopic surgery decreased the recovery time to TEN. This was in accordance with previous reports on routine cancer surgeries [6,7]. The length of postoperative hospital stay was, however, equivalent between the two groups. This is
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
most likely because of the fact that RE is associated with prolonged postoperative recovery as a result of malnutrition and mechanical intestinal obstruction. The deciding factor for recovery is the degree of radiation damage rather than surgical stress. Consequently, the advantage of minimal invasion cannot be translated to shortened hospital stay; however, it can be associated with enhanced surgical tolerance. RE represents a spectrum of clinical manifestations. One manifestation of chronic RE is REIIS. In this subgroup, the surgical strategy is relatively fixed with ileocecal resection proven to be associated with the best long-term prognosis [4]. The lesion is generally limited to the pelvic cavity. Consequently, the ports can be initiated similar to those in rectal operations. The greatest advantage of this fixed surgical strategy is its familiarity to gastrointestinal surgeons. The intricate nature of the procedure, dissection of the damaged intestines from the pelvic wall or sigmoid colon, requires great care, as injury to pelvic organs, such as the sigmoid colon or bladder, will usually result in the need for conversion. The conversion rate in the present study was 23.3% (7/30). The reason for conversion included strong adhesion in four cases and organ injuries in three cases. Strong adhesion beneath the anterior abdominal wall can affect the visual field and effect pneumoperitoneum and is therefore regarded a relative contraindication to laparoscopic surgery. A precise grading system is beneficial to both injury prophylaxis and decreasing the conversion rate. In the grading system used in the present study, both adhesion severity and distribution were taken into consideration. Grade 1 consisted of adhesion limited to the right lower abdomen with rare occurrence of sigmoid colon injury. However, retroperitoneal organ injury such as iliac vessels remained possible. Grades 2 and 3 were characterized by increased possibility of sigmoid colon and bladder injury, and grade 4 was usually the reason for conversion surgery, which was thus regarded as an absolute contraindication for laparoscopic surgery. Fibrosis and adhesion can be defined by preoperative CT scan. Therefore, a CT scan may be useful for preoperative grading. Further investigations on this subject would be beneficial to the development of laparoscopic surgery in REIIS.
5.
Conclusions
This is the first report on laparoscopic surgery for RE in English. As a preliminary report, this study demonstrated that laparoscopic surgery is feasible with a relatively low conversion rate and is as safe as open surgery on intraoperative and postoperative complications. In addition, laparoscopic surgery is superior to open surgery in terms of decreased skin incision length, operation time, intraoperative blood loss, and postoperative recovery to TEN.
Acknowledgment This work was supported by the following funding: National Natural Science Foundation of China (grant no. 81200327),
419
Natural Science Foundation of Jiangsu Province (grant no. BK2011415). Authors’ contributions: J.W. designed the study, wrote the article, and obtained the funding. D.Y., S.Z., and Q.M. collected data and did the analysis work. Y.L. and J.L. designed the study and critically revised the article.
Disclosure This work supported was obtained by J.W. The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
references
[1] Gidwani AL, Gardiner K, Clarke J. Surgical experience with small bowel damage secondary to pelvic radiotherapy. Ir J Med Sci 2009;178:13. [2] Theis VS, Sripadam R, Ramani V, Lal S. Chronic radiation enteritis. Clin Oncol 2010;22:70. [3] Kountouras J, Zavos C. Recent advances in the management of radiation colitis. World J Gastroenterol 2008;14:7289. [4] Lefevre JH, Amiot A, Joly F, et al. Risk of recurrence after surgery for chronic radiation enteritis. Br J Surg 2011;98:1792. [5] Rink AD, Fischer IR, Vestweber B, Vestweber KH. Long-term outcome of laparoscopic ileocecal resection for Crohn’s disease before the era of biologics. Int J Colorectal Dis 2014;29:127. [6] Boutros M, Hippalgaonkar N, Silva E, et al. Laparoscopic resection of rectal cancer results in higher lymph node yield and better short-term outcomes than open surgery: a large single-center comparative study. Dis Colon Rectum 2013; 56:679. [7] Yasunaga H, Horiguchi H, Kuwabara K, et al. Outcomes after laparoscopic or open distal gastrectomy for early-stage gastric cancer: a propensity-matched analysis. Ann Surg 2013;257:640. [8] Bismar MM, Sinicrope FA. Radiation enteritis. Curr Gastroenterol Rep 2002;4:361. [9] Onodera H, Nagayama S, Mori A, et al. Reappraisal of surgical treatment for radiation enteritis. World J Surg 2005;29:459. [10] Shibata D, Hyland W, Busse P, et al. Immediate reconstruction of the perineal wound with gracilis muscle flaps following abdominoperineal resection and intraoperative radiation therapy for recurrent carcinoma of the rectum. Ann Surg Oncol 1999;6:33. [11] Farid H, O’Connell TX. Methods to decrease the morbidity of abdominoperineal resection. Am Surg 1995;61:1061. [12] Wang J, Boerma M, Fu Q, Hauer-Jensen M. Radiation responses in skin and connective tissues: effect on wound healing and surgical outcome. Hernia 2006;10:502. [13] Itatsu K, Sugawara G, Kaneoka Y, et al. Risk factors for incisional surgical site infections in elective surgery for colorectal cancer: focus on intraoperative meticulous wound management. Surg Today 2014;44:1242. [14] Zhu W, Gong J, Li Y, et al. A retrospective study of surgical treatment of chronic radiation enteritis. J Surg Oncol 2012; 105:632. [15] Nielsen PH, Jepsen SB, Olsen AD. Postoperative pleural effusion following upper abdominal surgery. Chest 1989; 96:1133. [16] Zhe C, Jian-wei L, Jian C, et al. Laparoscopic versus open splenectomy and esophagogastric devascularization for bleeding varices or severe hypersplenism: a comparative study. J Gastrointest Surg 2013;17:654.
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Laparoscopic surgery for radiation enteritis Jian Wang, MD, PhD, Danhua Yao, MD, PhD, Shaoyi Zhang, MD, Qi Mao, MD, PhD, Yousheng Li, MD, PhD,* and Jieshou Li, MD, PhD Department of Surgery, Jinling Hospital, Nanjing University School of Medicine, Nanjing, China
article info
abstract
Article history:
Background: The aim of this study was to determine the safety and feasibility of laparo-
Received 29 August 2014
scopic surgery for radiation enteritis-induced intestinal stenosis requiring ileocecal
Received in revised form
resection.
30 October 2014
Methods: Clinical records of radiation enteritis patients that underwent laparoscopic ileo-
Accepted 14 November 2014
cecal resection and ileo-ascending colonic side-to-side anastomosis in a single center from
Available online 21 November 2014
January 2012eFebruary 2014 were retrospectively analyzed. Thirty patients were identified and matched by abdominal adhesion grade, age, gender, primary malignancy distribution,
Keywords:
previous abdominal surgery history, and body mass index to 30 patients that underwent
Laparoscopic surgery
open surgery for the same procedure from August 2009eDecember 2011. General infor-
Radiation enteritis
mation, operative findings, and short-term outcomes were compared between the two
Case-matched study
groups. Results: The conversion rate of laparoscopic surgery was 23.3%. The length of skin incision in the laparoscopic group was significantly shorter than that of the open surgery group (6.8 cm versus 15.8 cm, P ¼ 0.001). Laparoscopic surgery significantly decreased recovery time to total enteral nutrition (10.3 d versus 15.6 d, P ¼ 0.037); however, postoperative hospital stay was not significantly different between the two groups (28.2 d versus 32.4 d, P ¼ 0.924). Intraoperative blood loss (125 mL versus 189 mL, P ¼ 0.000) and operation time (138 min versus 171 min, P ¼ 0.003) were significantly improved in the laparoscopic group compared with those in the open surgery group. Laparoscopic surgery did not significantly decrease postoperative morbidity but did decrease the pleural effusion rate. Conclusions: Laparoscopic surgery is feasible for treatment of radiation enteritis-induced intestinal stenosis with a relatively low conversion rate. Laparoscopic surgery is as safe as open surgery and is superior to open surgery with decreased skin incision length, operation time, intraoperative blood loss, and postoperative recovery time to total enteral nutrition. ª 2015 Elsevier Inc. All rights reserved.
1.
Introduction
Radiation enteritis (RE) is an intestinal damage, represented by a spectrum of clinical manifestations, caused by abdominal or pelvic radiation. Surgical treatment is necessary for intestinal stenosis, intestinal perforation, and occasionally,
gastrointestinal hemorrhage [1]. Three to fifteen percent of RE patients will develop radiation enteritis-induced intestinal stenosis (REIIS) [2]. For REIIS, the surgical challenge lies in the dense intra-abdominal adhesion and fibrosis [3]. Postoperative complications including wound or anastomosis healing complications remain obstacles in traditional open
* Corresponding author. Department of Surgery, Jinling Hospital, Nanjing University School of Medicine, 305 East Zhongshan Road, Nanjing 210002, China. Tel.: þ86 25 8086 0137; fax: þ86 25 8541 9980. E-mail address: [email protected] (Y. Li). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2014.11.026
416
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
surgery [4]. The development of laparoscopic surgery has expanded the use of this technique from cholecystectomy to gastrointestinal cancer, and to other complicated inflammatory diseases such as Crohn disease [5] with the advantages of this technique simultaneously being identified. From 2012, the authors began to perform laparoscopic surgery for cases of RE. The aim of this study was to summarize the preliminary experience of laparoscopic surgery for REIIS and to determine the safety and feasibility of this technique.
2.
Materials and methods
2.1.
Patients
Laparoscopic surgery was introduced in our center on January 2012 by a team of surgeons. Clinical records of RE patients that presented with ileum stenosis and that underwent laparoscopic ileocecal resection and ileo-ascending colonic side-toside anastomosis from January 2012eFebruary 2014 were retrospectively reviewed. Patients that underwent open surgery for the same procedure in an earlier era, August 2009eDecember 2011 by the same unique team of surgeons, were 1:1 matched in terms of abdominal adhesion grade, age, gender, primary malignancy distribution, total radiation dose, interval between radiation and surgery, previous abdominal surgery history, and body mass index (BMI). All patients with REIIS in the two periods were considered for inclusion in this study. The exclusion criteria included emergent surgery, malignancy recurrence, preoperative short bowel syndrome (remnant small intestine <150 cm), or intraperitoneal chemotherapy history. The diagnosis was determined by clinical history, computed tomography (CT) manifestation, and confirmed by intraoperative and histologic findings. All patients presented with fibrosis and stenosis with the final 20 cm of the ileum affected. This was the pathologic basis of ileocecal resection [4]. All patients underwent preoperative parenteral or enteral nutritional support if they suffered malnutrition, as confirmed by low serum albumin levels. Operative findings and short-term outcomes were compared between the two groups including intraoperative blood loss; operation time; length and site of skin incision; conversion rate to open surgery; postoperative morbidity rate; recovery time to total enteral nutrition (TEN); and postoperative hospital stay. All surgical treatments were performed with informed signed consent, and the study was approved by the Medical Ethics Committee of Nanjing University.
2.2.
Operative techniques
For the laparoscopic group, when performing the dissection, a total laparoscopic technique was adopted. For all cases, four to five laparoscopic ports (5e12 mm in diameter) were used. A 12-mm supraumbilical port was used for the laparoscope and camera. The working ports included one 5-mm port placed in the right upper quadrant, one 5e12-mm port placed in the left upper quadrant, and a 12-mm trocar placed in the right iliac fossa. An additional 5-mm trocar was placed in the left iliac fossa if necessary. The ports were integrally moved 5 cm upward to be distant from previous incisions, if the previous
incisions expanded upward toward the navel. The first port was routinely made via the open method. Mobilization and dissection under a laparoscope was achieved using ultrasonic scissors (Ethicon Surgical Care, Somerville, NJ). After the exclusion of malignancy recurrence, the ileocecal and distal ileum were mobilized from the pelvic cavity, and blood supply of the lesion was discontinued by ultrasonic scissors or clips. After resection of the lesion, stapled ileo-ascending colonic side-to-side anastomosis was performed using staples (Ethicon Surgical Care) inside the abdomen or outside the abdomen with an adjuvant incision, which is in general on the upper abdomen for removing the intestinal lesion. Intraoperative bleeding was controlled by the use of metal clips or ultrasonic scissors. For open surgery, a lower-abdominal vertical or transverse incision was made for abdominal exposure. Dissection and anastomosis in these cases followed the same techniques as the laparoscopic surgery mentioned previously.
2.3.
Adhesion grading system
An intraperitoneal adhesion grading system specific to RE was initiated. The adhesion was divided into five grades as shown in Table 1. It should be noted that all adhesions discussed here are limited to adhesions between the intestines and the abdominal wall, pelvic wall, or pelvic contents. Adhesions among the intestinal lesions are not included as these cases required resection en bloc rather than lysis.
2.4.
Postoperative care
Parenteral nutrition was initiated on postoperative days 2e3. Simultaneously, enteral nutrition was administered through a nasogastric tube or gastrostoma. Parenteral nutrition was discontinued when enteral nutrition was achieved to full strength (25 kcal/kg/d). Postoperative complications were treated accordingly.
2.5.
Statistics
Results are presented as median (range) for quantitative outcomes and as frequencies for categorical outcomes. All outcomes were compared between the open surgery group and the laparoscopic surgery group. ManneWhitney tests for unpaired data were used for comparisons of age, total radiation
Table 1 e Adhesion grading system. Grade 0 1 2 3 4
Description No adhesion between the affected intestinal lesions and surrounding organs Adhesion and fibrosis limited to right pelvis Strong adhesion and fibrosis affecting whole pelvis, organs strongly attached with severe adhesions Grade 2 adhesion extending between intestine and anterior pelvic wall Grade 3 adhesion extending between intestine and anterior abdominal wall
417
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
Table 2 e General information of the patients. General information
Open surgery (n ¼ 30)
Laparoscopic surgery (n ¼ 30)
P value
52.1 (34e68) 2: 28
52.9 (34e71) 3: 27
0.761 1.000 0.844
18 6 5 1 52.9 (44e66) 34.8 (6e290) 27 19.9 (14.0e26.9)
17 4 6 3 51.2 (30e70) 32.4 (6e176) 30 19.0 (13.0e24.1)
Mean age (range, y) Gender (male: female) Primary malignancy Cervical carcinoma Endometrial cancer Rectal cancer Others Total radiation dose (Gy) Interval between radiation and surgery (mo) Number of patients with previous abdominal operations BMI (kg/cm2)
dose, interval between radiation and surgery, BMI, blood loss, operation time, length of skin incision, recovery time to TEN, and postoperative hospital stay. Chi-square tests were used for comparison of gender distribution, primary tumor distribution, previous abdominal surgery history, adhesion grade distribution, incision site distribution, and morbidity rate. All results were generated using SPSS statistical software (SPSS Inc, Chicago, IL). All tests were two-tailed, and P values of <0.05 were considered statistically significant.
3.
Results
Thirty patients were enrolled in the laparoscopic group and thirty patients were matched in the open surgery group. The groups were comparable for all matched factors including age; gender; primary malignancy distribution; previous abdominal surgery history; and BMI (Table 2). Abdominal adhesion grade was equivalent between the two groups (Table 3). Five intraoperative injuries occurred including two bladder injuries, two sigmoid colon injuries, and one external iliac artery injury (Table 4). All bladder injuries were successfully
repaired laparoscopically or under converted surgery during the operation without causing any postoperative complications. Sigmoid colon injuries were treated with preventative ileostomy. There was no significant difference between the two groups in terms of intraoperative injuries. Seven patients in the laparoscopic surgery group underwent conversion surgery. This was due to dense adhesion in four cases (grade 4 in three cases and grade 3 in one case), bladder injury in one case (grade 3), sigmoid colon injury in one case (grade 3), and external iliac artery injury in the final case (grade 1). Intraoperative blood loss and operation time were significantly lower in the laparoscopic group compared with those in the open surgery group. The skin incision length of the laparoscopic group was significantly shorter than that of the open surgery group (Table 3). In the 23 patients that underwent total laparoscopic surgery, 21 patients received a small right
Table 4 e Intraoperative injuries, postoperative morbidity, and short-term outcomes. Intra- and post-operative outcomes
Table 3 e Operative findings and results. Findings and results Adhesion grade 1 2 3 4 Intraoperative blood loss (mL) Operation time (min) Length of skin incision (cm) Incision Lower abdomen Upper abdomen Conversion rate NA ¼ not applicable.
Open surgery (n ¼ 30)
Laparoscopic surgery (n ¼ 30)
P value
7 12 9 2 189 (70e350)
10 6 11 3 125 (20e300)
0.000
171 (105e240)
138 (50e265)
0.003
15.8 (10e25)
6.8 (3e25)
0.001
30 0 NA
9 21 23.3%
0.403
0.000
NA
0.635 0.745 0.237 0.297
Intraoperative injuries Bladder Sigmoid colon External iliac artery Postoperative complications Incision infection or dehiscence Anastomotic leakage or fistula Pleural effusion Catheter Infection Cholestasis Abdominal bleeding Acute renal failure Recovery to TEN (postoperative day)* Postoperative hospital stay (d)* *
Open surgery Laparoscopic P value (n ¼ 30) surgery (n ¼ 30) 1 0 1 0 14
4 2 1 1 12
0.353 0.492 1.000 1.000 0.602
6
6
1.000
7
4
0.317
8 2 1 1 1 15.6 (4e61)
1 4 1 1 0 10.3 (4e22)
0.026 0.671 1.000 1.000 1.000 0.037
32.4 (13e111)
28.2 (12e56)
0.924
Patients with postoperative short bowel syndrome or ileostomy were not included.
418
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
Figure e Abdominal image from a patient who accepted a total laparoscopic procedure 6 mo ago. The lowerabdominal incision from a Dixon procedure performed 48 mo earlier failed to completely heal (white arrow), whereas the upper-right abdominal incision in laparoscopic surgery healed well (black arrow). (Color version of figure is available online.)
upper-abdominal incision (3e6 cm) and the remaining two patients received a right lower-abdominal incision that was previously an ileum stoma. No additional incision was made in these two patients. A total of 37 patients, including all patients in the open surgery group and the 7 patients that underwent conversed surgery in the laparoscopic group, received a lower-abdominal incision, with 19 patients receiving a transverse (10e20 cm) and 18 patients receiving vertical (8e25 cm) incisions. The general incision complication rate is presented in Table 4. A total of 11 of the 12 complications occurred in the lower-abdominal incisions, including 6 patients in the open surgery group, 4 patients that underwent conversed surgery, and 1 patient that underwent laparoscopic surgery. Only one incision complication occurred in an upper-abdominal incision. Figure is a representative image of a laparoscopic group case. The lower incision visible in the image was from a Dixon procedure conducted 48 mo earlier that failed to completely heal 6 mo after laparoscopic surgery, whereas the upper-abdominal incision from laparoscopic surgery healed well. Except for pleural effusion, there was no significant difference between the two groups in postoperative complications. Laparoscopic surgery significantly shortened the recovery time to TEN but did no decrease postoperative hospital stay (Table 4).
4.
Discussion
The short-term superiority of laparoscopic surgery has been well reported in routine gastrointestinal operation such as gastric or rectal cancer [6,7]. It is likely that this technique may also be advantageous in cases with more specific pathology,
such as RE. The intrinsic advantages of laparoscopic surgery (limited trauma, stress, and skin incision) make this procedure potentially beneficial to this group of patients that are generally characterized by malnutrition [8], incision complications, and uncertainty of malignancy recurrence. Although abdominal incisional complications are not as well defined as perineal wound after proctectomy, these complications remain the most common morbidity after radiation [9e11]. This is primarily due to abdominal wall damage as a result of the radiation [12]. In addition, wound length is a risk factor for wound infection in these patients [13]. Laparoscopic surgery can significantly shorten the incision length and can prevent the inclusion of the incision in the radiation field, which is generally conducted in the lower abdomen. This surgical strategy is promising to ultimately solve this incision problem. The data of the present study showed a significantly shorter incision length in the laparoscopic group; however, there was no significant difference in the rate of incision complications. There are four explanations for this inconsistency. First, the laparoscopic group included patients that underwent conversion surgery that resulted in four wound infections. Second, the laparoscopic group included one patient that failed to receive an incision in the healthy upper-abdominal wall. Third, the transverse incision was commonly used (17/30) in the open surgery group. Transverse incisions can partly move the incision away from the radiation field thereby possibly decreasing incision complications [14]. Finally, the sample size was relatively small, thus limiting interpretations of the data. The present study showed optimal results in operation time and intraoperative blood loss in the laparoscopic group. There was a significant decline in laparoscopic surgery operation time as cases growing (a decrease in time from 161 min for the first 15 procedures to 114 min for the second 15 procedures). The advantage of laparoscopic surgery in decreasing operation time is two-fold. First, pelvis exposure is improved in this technique allowing sharp, quick dissection and decreased blood loss. Second, the shortened incision in laparoscopic surgery significantly saves the time of abdominal closure. Laparoscopic surgery significantly decreased the rate of postoperative pleural effusion. Various factors are involved in the pathogenesis of nonspecific postoperative pleural effusion, including atelectasis, heart failure, transfusions during surgery, preoperative ascites, and hypoproteinemia, and so forth [15]. Few studies have compared the effect of laparoscopic surgery on postoperative pleural effusion. In one report, comparing the postoperative outcome between laparoscopic and open splenectomy and esophagogastric devascularization for bleeding varices or severe hypersplenism, lower pleural effusion was also found in the laparoscopic group [16]. In this article, the authors explained this result by improved postoperative physical activity in the laparoscopic group. In the present study, decreased skin incision length and pain may have also contributed to this improvement in postoperative outcomes. Laparoscopic surgery decreased the recovery time to TEN. This was in accordance with previous reports on routine cancer surgeries [6,7]. The length of postoperative hospital stay was, however, equivalent between the two groups. This is
j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 4 ( 2 0 1 5 ) 4 1 5 e4 1 9
most likely because of the fact that RE is associated with prolonged postoperative recovery as a result of malnutrition and mechanical intestinal obstruction. The deciding factor for recovery is the degree of radiation damage rather than surgical stress. Consequently, the advantage of minimal invasion cannot be translated to shortened hospital stay; however, it can be associated with enhanced surgical tolerance. RE represents a spectrum of clinical manifestations. One manifestation of chronic RE is REIIS. In this subgroup, the surgical strategy is relatively fixed with ileocecal resection proven to be associated with the best long-term prognosis [4]. The lesion is generally limited to the pelvic cavity. Consequently, the ports can be initiated similar to those in rectal operations. The greatest advantage of this fixed surgical strategy is its familiarity to gastrointestinal surgeons. The intricate nature of the procedure, dissection of the damaged intestines from the pelvic wall or sigmoid colon, requires great care, as injury to pelvic organs, such as the sigmoid colon or bladder, will usually result in the need for conversion. The conversion rate in the present study was 23.3% (7/30). The reason for conversion included strong adhesion in four cases and organ injuries in three cases. Strong adhesion beneath the anterior abdominal wall can affect the visual field and effect pneumoperitoneum and is therefore regarded a relative contraindication to laparoscopic surgery. A precise grading system is beneficial to both injury prophylaxis and decreasing the conversion rate. In the grading system used in the present study, both adhesion severity and distribution were taken into consideration. Grade 1 consisted of adhesion limited to the right lower abdomen with rare occurrence of sigmoid colon injury. However, retroperitoneal organ injury such as iliac vessels remained possible. Grades 2 and 3 were characterized by increased possibility of sigmoid colon and bladder injury, and grade 4 was usually the reason for conversion surgery, which was thus regarded as an absolute contraindication for laparoscopic surgery. Fibrosis and adhesion can be defined by preoperative CT scan. Therefore, a CT scan may be useful for preoperative grading. Further investigations on this subject would be beneficial to the development of laparoscopic surgery in REIIS.
5.
Conclusions
This is the first report on laparoscopic surgery for RE in English. As a preliminary report, this study demonstrated that laparoscopic surgery is feasible with a relatively low conversion rate and is as safe as open surgery on intraoperative and postoperative complications. In addition, laparoscopic surgery is superior to open surgery in terms of decreased skin incision length, operation time, intraoperative blood loss, and postoperative recovery to TEN.
Acknowledgment This work was supported by the following funding: National Natural Science Foundation of China (grant no. 81200327),
419
Natural Science Foundation of Jiangsu Province (grant no. BK2011415). Authors’ contributions: J.W. designed the study, wrote the article, and obtained the funding. D.Y., S.Z., and Q.M. collected data and did the analysis work. Y.L. and J.L. designed the study and critically revised the article.
Disclosure This work supported was obtained by J.W. The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
references
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