International Journal of Surgery 15 (2015) 79e83
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Laparoscopy-assisted combined resection for synchronous gastrointestinal multiple primary cancers Jia-feng Fang, Zong-heng Zheng, Yong Huang, Bo Wei, Jiang-long Huang, Pu-run Lei, Hong-bo Wei* Department of Gastrointestinal Surgery, The Third Affiliated Hospital of Sun Yat-sen University, Tianhe Road 600, Guangzhou 510630, China
h i g h l i g h t s Laparoscopy-assisted combined resection for SGMPC is feasible and safe. Laparoscopy-assisted combined resection for SGMPC is minimal invasive. Oncologic outcome laparoscopy-assisted combined resection for SGMPC is comparable.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 November 2014 Received in revised form 5 January 2015 Accepted 24 January 2015 Available online 29 January 2015
Background: Synchronous gastrointestinal multiple primary cancers (SGMPC) is infrequent. This study aimed to investigate the feasibility and outcomes of laparoscopy-assisted combined resection for SGMPC. Material and methods: We retrospectively reviewed 16 cases of SGMPC underwent either open or laparoscopy-assisted combined resection in the Third Affiliated Hospital of Sun Yat-sen University from Jan. 2005 to Jan. 2014. Results: Sixteen cases contained synchronous colon cancers (n ¼ 10), gastric and rectal cancer (n ¼ 5), gastric and duodenal cancer (n ¼ 1). Either laparoscopy-assisted or open procedure was performed. Compared with the open group, the laparoscopy group presented less blood loss (77.1 ± 46.3 ml vs. 145.0 ± 75.9 ml, P ¼ 0.047) and shorter incision length (5.2 ± 0.7 cm vs. 16.4 ± 1.9 cm, P ¼ 0.000), while no differences in operative time (228.3 ± 38.8 min vs. 188.8 ± 47.7 min, P > 0.05) and postoperative hospital stay (10.0 ± 3.4 days vs. 12.0 ± 4.8 days, P > 0.05). Two cases of postoperative complications occurred in the open group and one case of incision infection occurred in the laparoscopy one. Upon follow-up, 2 cases of open group (50.0%) and 8 cases of laparoscopy group (66.7%) were under status of disease free survival. Conclusions: Laparoscopy-assisted combined resection for SGMPC is feasible, safe and effective. © 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
Keywords: Multiple primary cancers Synchronous Gastrointestinal Laparoscopy
1. Introduction Multiple primary cancers (MPC) is a rare condition defined as two or more different tumors synchronously or metachronously forming in the same individual [1]. Synchronous gastrointestinal multiple primary cancers (SGMPC) is even infrequent, and its surgical treatment remains poorly understood. Nowadays, laparoscopy-assisted surgery is widely applied in single primary gastrointestinal cancer. The outcomes appear better compared with those via the open approach [2e4]. However, whether laparoscopy-
assisted combined resection for SGMPC is still feasible and comparable to the open one is still elusive. In this study, we aimed to investigate the feasibility and outcomes of simultaneous laparoscopy-assisted combined resection for SGMPC. To our knowledge, so far our study contained maximum cases of SGMPC underwent laparoscopy surgery.
2. Materials and methods 2.1. Patient selection
* Corresponding author. E-mail address: [email protected] (H.-b. Wei). http://dx.doi.org/10.1016/j.ijsu.2015.01.021 1743-9191/© 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
The diagnostic criteria of multiple primary gastrointestinal cancers drawn up by Warren and Gates are as follows [5]: firstly,
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each gastrointestinal tumor should be histopathologically malignant; secondly, each tumor should be histologically different; thirdly, the possibility of metastasis of each tumor should be ruled out. The criterion for a tumor's being “synchronous” or “metachronous” is within 6 months or not. From Jan. 2005 to Jan. 2014, 2565 cases of patients were diagnosed as primary gastrointestinal cancer in the Third Affiliated Hospital of Sun Yat-sen University. 27 cases of them were diagnosed as SGMPC. Among these 27 cases, 2 cases refused to accept surgery, 9 cases were diagnosed with synchronous sigmoid and rectal cancer and underwent single open or laparoscopy-assisted proctosigmoidectomy, while the other 16 cases underwent simultaneous combined resection for cancers. We retrospectively reviewed records of these 16 cases, containing 4 cases of open resection and 12 cases of laparoscopy-assisted combined resection. 2.2. Data collection Patient demographics, clinical history, laboratory data, imaging results and surgery data were obtained through review of computerized medical records. SGMPC were diagnosed by combination of gastrointestinal endoscopy, biopsy and CT scan of abdomen. Pre-operative TNM staging revealed 4 cases of Stage II, 11 cases of Stage III and 1 case of Stage IV (TNM stage was indentified according to the worse one of the multiple primary cancers). The main outcome measures contained operative time, blood loss, postoperative morbidity, postoperative hospital stay and mortality. 2.3. Follow-up Follow-up was carried out at every 3 months in the first two years postoperatively, 6 months in the third year and 12 months later, containing contents of history collecting, physical examination, laboratory and imaging tests. Outpatient follow-up, E-mail or telephone survey were conducted to collect follow-up status. The last follow-up was finished in Mar. 2014. 2.4. Statistical analyses Continuous data were expressed as mean ± SD and compared with Student's t test. Categorical data were expressed as frequency
and compared with chi-square test or fisher exact test. All P-values were two-sided, and the statistical significant level was 0.05. Statistical analyses were conducted using the SPSS software package version 11.0 (Chicago, IL, United States).
2.5. Operative procedure We studied details of laparoscopy-assisted combined resection for SGMPC. Different procedures of laparoscopy-assisted combined resection were performed according to the location of SGMPC (Table 1). Here, we took laparoscopy-assisted combined distal gastrectomy and low anterior resection for example, to describe the brief procedure as follows. The operation was performed under general anesthesia. The patient was firstly placed in lithotomy position to finish the low anterior resection. A Veress needle was used to establish pneumoperitoneum and the intra-abdominal pressure was maintained at the level of 14 mmHg. A 10 mm trocar (A) was placed below the umbilicus for a 30-degree telescope and another three trocars (B 12 mm, C 5 mm, D 5 mm) were placed for manipulation at the McBurney's point, left and right lateral sides of the rectus abdominis at the level of umbilicus respectively. The surgeons and monitor were positioned as shown in Fig. 1. The sigmoid mesocolon and mesorectum were dissected along the inner side of ureter by harmonic scalpel. The vessel and lymphatic were ligated at the root of the inferior mesenteric vessel with polymer clips, and the distal rectum was transected intracorporeally with a 60 mm laparoscopic linear stapler. Then the patient was turned into Trendelenburg position and another trocar (E 12 mm) was placed at the crossing point of the left costal margin and anterior axillary line to complete the lymph node dissection and distal gastrectomy. The surgeons and monitor changed positions as shown in Fig. 2. Firstly, the greater omentum, together with the frontal layer of transverse mesocolon, pancreatic capsule and No.4 lymph nodes were dissected from the splenic flexure to hepatic flexure. The left and right gastroepiploic vessels were ligated and No.6 lymph nodes were dissected simultaneously. Then the hepatoduodenal ligament and No.12 lymph nodes were dissected. Afterwards, the right gastric vessel and left gastric vessel were ligated gradually, together with the dissection of No.5, No.7, No.8 and No.9 lymph nodes respectively. After dissection of No.1
Table 1 Operative procedure and data. Case
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 a b c d
Tumor locationa
GC þ RC IC þ RC HFC þ RC HFC þ RC GC þ RC IC þ RC SFC þ RC GC þ RC HFC þ RC GC þ RC SFC þ RC HFC þ RC GC þ RC GC þ DC SFC þ RC SFC þ RC
Pre-operative TNM staging
II II III II III III III III III III II IV III III III III
Operative procedure Methodb
Resectionc
Anastomosisd
Operative time (min)
Blood loss (ml)
O O L L O L L L O L L L L L L L
DG þ LAR RH þ LAR RH þ LAR RH þ LAR DG þ LAR RH þ LAR LH þ LAR DG þ LAR RH þ LAR DG þ LAR LH þ LAR RH þ LAR DG þ LAR DG þ PD LH þ LAR LH þ LAR
Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler,
245 160 245 230 210 215 205 260 140 255 250 195 245 300 175 165
250 100 100 30 150 100 75 60 80 80 50 100 30 200 50 50
extra extra extra extra extra extra extra extra extra extra extra extra extra extra extra extra
GC, gastric cancer; RC, rectal cancer; IC, ileocecal cancer; HFC, hepatic flexure colon cancer; SFC, splenic flexure colon cancer; DC, duodenal cancer. O, open surgery; L, laparoscopy-assisted surgery. DG, distal gastrectomy; LAR, low anterior resection; RH, right hemicolectomy; LH, left hemicolectomy; PD, pancreaticoduodenectomy. extra, extra-corporeal anastomosis.
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3. Results 3.1. Patient characteristics
Fig. 1. First step of laparoscopy-assisted combined distal gastrectomy and low anterior resection to finish the low anterior resection. The patient was placed in lithotomy position. 10 mm trocar (A) was placed below the umbilicus for a 30-degree telescope and another three trocars (B 12 mm, C 5 mm, D 5 mm) were placed for manipulation at the McBurney's point, left and right lateral sides of the rectus abdominis at the level of umbilicus respectively. The monitor was positioned between the legs of patient. Operator stood in the right side of patient, while camera surgeon an assistant surgeon stood in the left side.
and No.3 lymph nodes, the stomach was totally mobilized with an adequate perigastric lymphadenectomy. The distal stomach and first portion of duodenum were also transected intracorporeally with a 60 mm laparoscopic linear stapler. A 5 cm median epigastric incision was made to remove specimens containing the proximal rectum, the distal stomach and first portion of duodenum, the surrounding tissues of the rectum and stomach. A Billroth II reconstruction with 25 mm intraluminal stapler was completed extracorporeally for gastric cancer. Correspondingly, the sigmoidorectostomy was completed with 29 mm intraluminal stapler intracorporeally.
There were 16 patients diagnosed with SGMPC and underwent simultaneous combined resection. These 16 cases contained 10 cases of synchronous colon cancers (4 cases of hepatic flexure colon and rectal cancer, 4 cases of splenic flexure colon and rectal cancer, and 2 cases of ileocecal and rectal cancer), 5 cases of synchronous gastric and rectal cancer, and one case of synchronous gastric and duodenal cancer. Sixteen cases contained 6 male and 10 female, age ranged from 24 to 86 years, with a mean age of 61.3 years. BMI ranged from 16.6 to 27.6 kg/m2. The most frequent symptom was abnormal defecation (n ¼ 11), and other symptoms included abdominal pain (n ¼ 7), lose weight (n ¼ 4), abdominal mass (n ¼ 2) and dizzy (n ¼ 1). Serum tumor markers were detected. The results showed 6 cases of elevated CEA level, 5 cases of elevated CA19-9 level and 3 cases of simultaneous elevated CEA and CA19-9 levels. Four cases underwent open combined resection for SGMPC while the other 12 cases underwent laparoscopy-assisted surgery. The patients’ characteristics had no significant differences between the open group and laparoscopy group (Table 2). 3.2. Surgery data The surgical interventions were managed according to location of SGMPC. The open group contained 2 cases of sub-total colorectal resection (combined right hemicolectomy and low anterior resection) and 2 cases of combined distal gastrectomy and low anterior resection. The mean operative time and blood loss were 188.8 ± 47.7 min and 145.0 ± 75.9 ml, respectively. The mean incision length and postoperative hospital stay were 16.4 ± 1.9 cm and 12.0 ± 4.8 days, respectively. Two cases of postoperative complications (pulmonary infection and incision infection respectively) occurred and were cured later. No postoperative mortality occurred. The laparoscopy group contained 8 cases of laparoscopyassisted sub-total colorectal resection (4 cases of right hemicolectomy and low anterior resection, 4 cases of left hemicolectomy and low anterior resection), 3 cases of laparoscopy-assisted combined distal gastrectomy and low anterior resection, and one case of laparoscopy-assisted combined distal gastrectomy and pancreaticoduodenectomy. No patient underwent conversion to laparotomy. Compared with the open group, the laparoscopy group presented less blood loss (77.1 ± 46.3 ml, P ¼ 0.047) and shorter incision length (5.2 ± 0.7 cm, P ¼ 0.000), while no differences in operative time (228.3 ± 38.8 min, P > 0.05) and postoperative Table 2 Patient characteristics. Group
Gender Male Female
4
59.5 ± 15.4 1
3
Laparoscopy 12
62.3 ± 15.8 5
7
Open
Fig. 2. Second step of laparoscopy-assisted combined distal gastrectomy and low anterior resection to complete the lymph node dissection and distal gastrectomy. The patient was turned into Trendelenburg position and another trocar (E 12 mm) was placed at the crossing point of the left costal margin and anterior axillary line. The monitors changed to be positioned on the head side of patient. The operator changed to stand in the left side of patient, while the assistant surgeon in the right side. The camera surgeon stood between legs of patient.
Case Mean age (years)
P value a
e
>0.05
>0.05
BMI (kg/m2)
Tumor locationa Case
21.2 ± 3.4 Colon cancersb GC and RC 21.5 ± 3.1 Colon cancersc GC and RC GC and DC >0.05 e
2 2 8 3 1 e
GC, gastric cancer; RC, rectal cancer; DC, duodenal cancer. b Colon cancers, containing one case of synchronous HFC (hepatic flexure colon cancer) and RC, and one case of IC (ileocecal cancer) and RC. c Colon cancers, containing 4 cases of synchronous SFC (splenic flexure colon cancer) and RC, 3 cases of HFC and RC, 1 case of IC and RC.
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hospital stay (10.0 ± 3.4 days, P > 0.05). One case of incision infection occurred postoperatively and was cured later. No postoperative mortality occurred either (Table 3) 3.3. Pathological data The specimens were confirmed by histologic diagnosis. In the open group, median numbers of lymph nodes harvested and positive were 34.3 ± 8.2 and 1.9 ± 1.5 respectively. The positive rate of lymph nodes was 5.4%. On the contrast, in laparoscopy group, the results were 39.0 ± 7.9, 3.0 ± 2.9 and 7.7% respectively. TNM stage revealed 2 cases of Stage II and 2 cases of Stage III (TNM stage was indentified according to the worse one of the multiple primary cancers) in open group. The situations in laparoscopy group were 2 cases of Stage II, 9 cases of Stage III and 1 cases of Stage IV (Table 4). 3.4. Follow-up status According to results of TNM stage, adjuvant therapy was unnecessary for 3 patients, while the other 13 patients were recommended to accept adjuvant therapy. Eleven patients underwent adjuvant therapy containing chemotherapy and radiotherapy (if necessary), while 2 patients refused adjuvant therapy. Follow-up was completed in all 16 patients for 28.7 ± 21.2 months. The results revealed 10 cases of disease free survival, 4 cases of residual disease survival and 2 cases of cancer-related death. The mortality rate was 12.5% according to the last followup result (Table 3). 4. Discussion Multiple primary cancers (MPC) can be defined as two or more different tumors synchronously or metachronously forming in the same individual. It was first described by Billroth in 1889, while its diagnostic criteria were drawn up by Warren and Gates in 1932 [5]. Then Moertel [6] categorized MPC into three groups: tumors formed in the same organ, tumors formed in different organs, and the combination of the first two cases. The incidence of MPC is low, ranging between 0.5% and 3% in China, which is much lower than that of other counties and it may be due to the unawareness and inferiority of diagnostic level [7,8]. Synchronous gastrointestinal multiple primary cancers (SGMPC) is even rare [9,10]. A prospective study revealed that 19 cases of 543 gastric cancers developed colorectal cancer synchronously [11]. Another retrospective study demonstrated 35 cases of 4426 gastric cancers developed colorectal cancer, while only 3 cases occurred synchronously [12]. In this study, the proportion of 27 cases of SGMPC in gastrointestinal primary cancers was 1.1%. These 27 cases were diagnosed by combination of gastrointestinal endoscopy and CT scan of abdomen. PET/CT was also recommended
for diagnosis of SGMPC in some cases [13]. Surgical intervention is the first option for SGMPC. However, simultaneous surgical resection indicates more difficulties and higher operation risk than surgical resection for single cancer. Take synchronous rectal and gastric cancer for example, conventional open resection requires a wide incision from xiphoid to the pubic symphysis, and may lead to a poor cosmetic result and impaired quality of postoperative life. Meanwhile, severe trauma may result in postoperative complications and a delayed recovery. Nowadays, laparoscopy surgery has been performed worldwide. Laparoscopy-assisted colorectal resection has been advocated as a standard treatment for colorectal cancer because of less trauma and faster recovery without sacrificing similar oncological outcome [14,15]. Long-term outcomes of laparoscopic distal gastrectomy for advanced gastric cancer have also been proved by some studies [16,17]. Therefore, simultaneous laparoscopy-assisted resection for SGMPC is feasible in theory. This assumption is supported by some case reports. One case of esophageal cancer with sigmoid colon cancer treated by laparoscopic surgery and another case of laparoscopic resection of sporadic synchronous gastric and jejunal gastrointestinal stromal tumors have been reported [18,19]. In addition, several cases of simultaneous laparoscopy-assisted resection for synchronous rectal and gastric cancer have been reported, and the results revealed a fast recovery, low incidence of complication and a good cosmetic result [20e22]. Experience of performing numerous laparoscopy-assisted surgeries enhanced our confidence to perform simultaneous laparoscopy-assisted resection for SGMPC. Instead of a wide incision, several small incisions were made for trocars’ placements to finish multiple tumors resection and lymphadenectomy. A median 5 cm of assisted incision was applied to remove specimen and finish digestive reconstruction. Thus, a better cosmetic result and less blood loss were guaranteed. These advantages were even significant in patients diagnosed with synchronous gastric and rectal cancer [23]. In this study, totally 5 cases of synchronous gastric and rectal cancer were included, containing 3 cases of laparoscopy surgery and 2 cases of open resection. Compared to open resection, laparoscopy-assisted combined distal gastrectomy and low anterior resection presented advantages of less blood loss (56.7 ± 25.2 vs. 200.0 ± 70.7 ml), shorter incision length (5.0 ± 0.0 vs. 19.0 ± 1.4 cm) and postoperative hospital stay (12.3 ± 2.1 vs. 17.0 ± 4.2 days). However, more cases and prospectively study, if possible, are needed to further confirm the advantages. The oncological outcomes were also discussed in our study and the results seemed satisfactory. Median number of lymph nodes harvested was equal in laparoscopy and open group. Disease free survival rate seemed better in laparoscopy group. However, due to shorter follow-up time of laparoscopy group, whether oncological outcomes of simultaneous laparoscopy-assisted resection for SGMPC is similar to the open one still need confirmation by more cases and long-term follow-up.
Table 3 Surgery data. Group
Operative methoda
Case
Operative time (min)
Blood loss (ml)
Incision length (cm)
Postoperative hospital stay (days)
Open
STCR DG þ LAR LASTCR LADG þ LALAR LADG þ LAPD e
2 2 8 3 1 e
188.8 ± 47.7
145.0 ± 75.9
16.4 ± 1.9
12.0 ± 4.8
2
228.3 ± 38.8
77.1 ± 46.3
5.2 ± 0.7
10.0 ± 3.4
1
>0.05
0.047
0.000
>0.05
Laparoscopy
P value a
Postoperative complications (case)
>0.05
STCR, sub-total colorectal resection; DG, distal gastrectomy; LAR, low anterior resection; LASTCR, Laparoscopy-assisted sub-total colorectal resection; LADG, Laparoscopyassisted distal gastrectomy; LALAR, Laparoscopy-assisted low anterior resection; LAPD, Laparoscopy-assisted pancreaticoduodenectomy.
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Table 4 Oncological outcome. Group
Open Laparoscopy P value a
Lymph nodes
TNM stage
Harvested
Positive
34.3 ± 8.2 39.0 ± 7.9 >0.05
1.9 ± 1.5 3.0 ± 2.9 >0.05
II 2 2 >0.05
Follow-up (months) III
IV
2 9
e 1
46.8 ± 29.4 23.7 ± 14.8 >0.05
Statusa DFS
RDS
CRD
2 8
1 3
1 1
DFS, Disease free survival; RDS, residual disease survival; CRD, cancer-related death.
In our experience, some key points should be paid attention to during performing simultaneous laparoscopy-assisted resection for SGMPC. First, surgeon should have plentiful experience in laparoscopy surgery. Second, surgeon should be familiar with the anatomy of gastrointestinal tract and its surrounding tissues. Third, the operator, camera surgeon and monitor should change positions timely when turning dissection of one cancer to another. Last, trocar placement should be well designed before surgery and surgeon should not hesitate to add another trocar when facing with difficult operation. Take laparoscopy-assisted combined distal gastrectomy and low anterior resection for example. When we performed laparoscopy-assisted low anterior resection first, the positions of trocars were designed nearer the head side than usual so that these trocars could be used for operation of distal gastrectomy. 5. Conclusion To our knowledge, so far our study contains maximum cases of SGMPC underwent laparoscopy surgery. SGMPC is rare and difficult to involved in cohort study, so we believe a report of 12 patients underwent laparoscopy surgery is useful even though it is a retrospective study and exist bias. Our study revealed that performed by surgeons experienced in laparoscopy surgery, laparoscopy-assisted combined resection for SGMPC is feasible, safe and effective. However, more cases and long-term follow-up are needed to confirm the surgical advantages and similar oncological outcomes. Ethical approval None. Sources of funding None. Author contribution Designed the study: Hong-bo and Jia-feng. Performed surgery: Hong-bo, Zong-heng, Jiang-long and Yong. Acquisition of data: Jiafeng and Pu-run. Analyzed the data: Bo. Wrote the paper: Jia-feng and Bo. Conflicts of interest None. Guarantor None.
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Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Laparoscopy-assisted combined resection for synchronous gastrointestinal multiple primary cancers Jia-feng Fang, Zong-heng Zheng, Yong Huang, Bo Wei, Jiang-long Huang, Pu-run Lei, Hong-bo Wei* Department of Gastrointestinal Surgery, The Third Affiliated Hospital of Sun Yat-sen University, Tianhe Road 600, Guangzhou 510630, China
h i g h l i g h t s Laparoscopy-assisted combined resection for SGMPC is feasible and safe. Laparoscopy-assisted combined resection for SGMPC is minimal invasive. Oncologic outcome laparoscopy-assisted combined resection for SGMPC is comparable.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 November 2014 Received in revised form 5 January 2015 Accepted 24 January 2015 Available online 29 January 2015
Background: Synchronous gastrointestinal multiple primary cancers (SGMPC) is infrequent. This study aimed to investigate the feasibility and outcomes of laparoscopy-assisted combined resection for SGMPC. Material and methods: We retrospectively reviewed 16 cases of SGMPC underwent either open or laparoscopy-assisted combined resection in the Third Affiliated Hospital of Sun Yat-sen University from Jan. 2005 to Jan. 2014. Results: Sixteen cases contained synchronous colon cancers (n ¼ 10), gastric and rectal cancer (n ¼ 5), gastric and duodenal cancer (n ¼ 1). Either laparoscopy-assisted or open procedure was performed. Compared with the open group, the laparoscopy group presented less blood loss (77.1 ± 46.3 ml vs. 145.0 ± 75.9 ml, P ¼ 0.047) and shorter incision length (5.2 ± 0.7 cm vs. 16.4 ± 1.9 cm, P ¼ 0.000), while no differences in operative time (228.3 ± 38.8 min vs. 188.8 ± 47.7 min, P > 0.05) and postoperative hospital stay (10.0 ± 3.4 days vs. 12.0 ± 4.8 days, P > 0.05). Two cases of postoperative complications occurred in the open group and one case of incision infection occurred in the laparoscopy one. Upon follow-up, 2 cases of open group (50.0%) and 8 cases of laparoscopy group (66.7%) were under status of disease free survival. Conclusions: Laparoscopy-assisted combined resection for SGMPC is feasible, safe and effective. © 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
Keywords: Multiple primary cancers Synchronous Gastrointestinal Laparoscopy
1. Introduction Multiple primary cancers (MPC) is a rare condition defined as two or more different tumors synchronously or metachronously forming in the same individual [1]. Synchronous gastrointestinal multiple primary cancers (SGMPC) is even infrequent, and its surgical treatment remains poorly understood. Nowadays, laparoscopy-assisted surgery is widely applied in single primary gastrointestinal cancer. The outcomes appear better compared with those via the open approach [2e4]. However, whether laparoscopy-
assisted combined resection for SGMPC is still feasible and comparable to the open one is still elusive. In this study, we aimed to investigate the feasibility and outcomes of simultaneous laparoscopy-assisted combined resection for SGMPC. To our knowledge, so far our study contained maximum cases of SGMPC underwent laparoscopy surgery.
2. Materials and methods 2.1. Patient selection
* Corresponding author. E-mail address: [email protected] (H.-b. Wei). http://dx.doi.org/10.1016/j.ijsu.2015.01.021 1743-9191/© 2015 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
The diagnostic criteria of multiple primary gastrointestinal cancers drawn up by Warren and Gates are as follows [5]: firstly,
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each gastrointestinal tumor should be histopathologically malignant; secondly, each tumor should be histologically different; thirdly, the possibility of metastasis of each tumor should be ruled out. The criterion for a tumor's being “synchronous” or “metachronous” is within 6 months or not. From Jan. 2005 to Jan. 2014, 2565 cases of patients were diagnosed as primary gastrointestinal cancer in the Third Affiliated Hospital of Sun Yat-sen University. 27 cases of them were diagnosed as SGMPC. Among these 27 cases, 2 cases refused to accept surgery, 9 cases were diagnosed with synchronous sigmoid and rectal cancer and underwent single open or laparoscopy-assisted proctosigmoidectomy, while the other 16 cases underwent simultaneous combined resection for cancers. We retrospectively reviewed records of these 16 cases, containing 4 cases of open resection and 12 cases of laparoscopy-assisted combined resection. 2.2. Data collection Patient demographics, clinical history, laboratory data, imaging results and surgery data were obtained through review of computerized medical records. SGMPC were diagnosed by combination of gastrointestinal endoscopy, biopsy and CT scan of abdomen. Pre-operative TNM staging revealed 4 cases of Stage II, 11 cases of Stage III and 1 case of Stage IV (TNM stage was indentified according to the worse one of the multiple primary cancers). The main outcome measures contained operative time, blood loss, postoperative morbidity, postoperative hospital stay and mortality. 2.3. Follow-up Follow-up was carried out at every 3 months in the first two years postoperatively, 6 months in the third year and 12 months later, containing contents of history collecting, physical examination, laboratory and imaging tests. Outpatient follow-up, E-mail or telephone survey were conducted to collect follow-up status. The last follow-up was finished in Mar. 2014. 2.4. Statistical analyses Continuous data were expressed as mean ± SD and compared with Student's t test. Categorical data were expressed as frequency
and compared with chi-square test or fisher exact test. All P-values were two-sided, and the statistical significant level was 0.05. Statistical analyses were conducted using the SPSS software package version 11.0 (Chicago, IL, United States).
2.5. Operative procedure We studied details of laparoscopy-assisted combined resection for SGMPC. Different procedures of laparoscopy-assisted combined resection were performed according to the location of SGMPC (Table 1). Here, we took laparoscopy-assisted combined distal gastrectomy and low anterior resection for example, to describe the brief procedure as follows. The operation was performed under general anesthesia. The patient was firstly placed in lithotomy position to finish the low anterior resection. A Veress needle was used to establish pneumoperitoneum and the intra-abdominal pressure was maintained at the level of 14 mmHg. A 10 mm trocar (A) was placed below the umbilicus for a 30-degree telescope and another three trocars (B 12 mm, C 5 mm, D 5 mm) were placed for manipulation at the McBurney's point, left and right lateral sides of the rectus abdominis at the level of umbilicus respectively. The surgeons and monitor were positioned as shown in Fig. 1. The sigmoid mesocolon and mesorectum were dissected along the inner side of ureter by harmonic scalpel. The vessel and lymphatic were ligated at the root of the inferior mesenteric vessel with polymer clips, and the distal rectum was transected intracorporeally with a 60 mm laparoscopic linear stapler. Then the patient was turned into Trendelenburg position and another trocar (E 12 mm) was placed at the crossing point of the left costal margin and anterior axillary line to complete the lymph node dissection and distal gastrectomy. The surgeons and monitor changed positions as shown in Fig. 2. Firstly, the greater omentum, together with the frontal layer of transverse mesocolon, pancreatic capsule and No.4 lymph nodes were dissected from the splenic flexure to hepatic flexure. The left and right gastroepiploic vessels were ligated and No.6 lymph nodes were dissected simultaneously. Then the hepatoduodenal ligament and No.12 lymph nodes were dissected. Afterwards, the right gastric vessel and left gastric vessel were ligated gradually, together with the dissection of No.5, No.7, No.8 and No.9 lymph nodes respectively. After dissection of No.1
Table 1 Operative procedure and data. Case
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 a b c d
Tumor locationa
GC þ RC IC þ RC HFC þ RC HFC þ RC GC þ RC IC þ RC SFC þ RC GC þ RC HFC þ RC GC þ RC SFC þ RC HFC þ RC GC þ RC GC þ DC SFC þ RC SFC þ RC
Pre-operative TNM staging
II II III II III III III III III III II IV III III III III
Operative procedure Methodb
Resectionc
Anastomosisd
Operative time (min)
Blood loss (ml)
O O L L O L L L O L L L L L L L
DG þ LAR RH þ LAR RH þ LAR RH þ LAR DG þ LAR RH þ LAR LH þ LAR DG þ LAR RH þ LAR DG þ LAR LH þ LAR RH þ LAR DG þ LAR DG þ PD LH þ LAR LH þ LAR
Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler, Stapler,
245 160 245 230 210 215 205 260 140 255 250 195 245 300 175 165
250 100 100 30 150 100 75 60 80 80 50 100 30 200 50 50
extra extra extra extra extra extra extra extra extra extra extra extra extra extra extra extra
GC, gastric cancer; RC, rectal cancer; IC, ileocecal cancer; HFC, hepatic flexure colon cancer; SFC, splenic flexure colon cancer; DC, duodenal cancer. O, open surgery; L, laparoscopy-assisted surgery. DG, distal gastrectomy; LAR, low anterior resection; RH, right hemicolectomy; LH, left hemicolectomy; PD, pancreaticoduodenectomy. extra, extra-corporeal anastomosis.
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3. Results 3.1. Patient characteristics
Fig. 1. First step of laparoscopy-assisted combined distal gastrectomy and low anterior resection to finish the low anterior resection. The patient was placed in lithotomy position. 10 mm trocar (A) was placed below the umbilicus for a 30-degree telescope and another three trocars (B 12 mm, C 5 mm, D 5 mm) were placed for manipulation at the McBurney's point, left and right lateral sides of the rectus abdominis at the level of umbilicus respectively. The monitor was positioned between the legs of patient. Operator stood in the right side of patient, while camera surgeon an assistant surgeon stood in the left side.
and No.3 lymph nodes, the stomach was totally mobilized with an adequate perigastric lymphadenectomy. The distal stomach and first portion of duodenum were also transected intracorporeally with a 60 mm laparoscopic linear stapler. A 5 cm median epigastric incision was made to remove specimens containing the proximal rectum, the distal stomach and first portion of duodenum, the surrounding tissues of the rectum and stomach. A Billroth II reconstruction with 25 mm intraluminal stapler was completed extracorporeally for gastric cancer. Correspondingly, the sigmoidorectostomy was completed with 29 mm intraluminal stapler intracorporeally.
There were 16 patients diagnosed with SGMPC and underwent simultaneous combined resection. These 16 cases contained 10 cases of synchronous colon cancers (4 cases of hepatic flexure colon and rectal cancer, 4 cases of splenic flexure colon and rectal cancer, and 2 cases of ileocecal and rectal cancer), 5 cases of synchronous gastric and rectal cancer, and one case of synchronous gastric and duodenal cancer. Sixteen cases contained 6 male and 10 female, age ranged from 24 to 86 years, with a mean age of 61.3 years. BMI ranged from 16.6 to 27.6 kg/m2. The most frequent symptom was abnormal defecation (n ¼ 11), and other symptoms included abdominal pain (n ¼ 7), lose weight (n ¼ 4), abdominal mass (n ¼ 2) and dizzy (n ¼ 1). Serum tumor markers were detected. The results showed 6 cases of elevated CEA level, 5 cases of elevated CA19-9 level and 3 cases of simultaneous elevated CEA and CA19-9 levels. Four cases underwent open combined resection for SGMPC while the other 12 cases underwent laparoscopy-assisted surgery. The patients’ characteristics had no significant differences between the open group and laparoscopy group (Table 2). 3.2. Surgery data The surgical interventions were managed according to location of SGMPC. The open group contained 2 cases of sub-total colorectal resection (combined right hemicolectomy and low anterior resection) and 2 cases of combined distal gastrectomy and low anterior resection. The mean operative time and blood loss were 188.8 ± 47.7 min and 145.0 ± 75.9 ml, respectively. The mean incision length and postoperative hospital stay were 16.4 ± 1.9 cm and 12.0 ± 4.8 days, respectively. Two cases of postoperative complications (pulmonary infection and incision infection respectively) occurred and were cured later. No postoperative mortality occurred. The laparoscopy group contained 8 cases of laparoscopyassisted sub-total colorectal resection (4 cases of right hemicolectomy and low anterior resection, 4 cases of left hemicolectomy and low anterior resection), 3 cases of laparoscopy-assisted combined distal gastrectomy and low anterior resection, and one case of laparoscopy-assisted combined distal gastrectomy and pancreaticoduodenectomy. No patient underwent conversion to laparotomy. Compared with the open group, the laparoscopy group presented less blood loss (77.1 ± 46.3 ml, P ¼ 0.047) and shorter incision length (5.2 ± 0.7 cm, P ¼ 0.000), while no differences in operative time (228.3 ± 38.8 min, P > 0.05) and postoperative Table 2 Patient characteristics. Group
Gender Male Female
4
59.5 ± 15.4 1
3
Laparoscopy 12
62.3 ± 15.8 5
7
Open
Fig. 2. Second step of laparoscopy-assisted combined distal gastrectomy and low anterior resection to complete the lymph node dissection and distal gastrectomy. The patient was turned into Trendelenburg position and another trocar (E 12 mm) was placed at the crossing point of the left costal margin and anterior axillary line. The monitors changed to be positioned on the head side of patient. The operator changed to stand in the left side of patient, while the assistant surgeon in the right side. The camera surgeon stood between legs of patient.
Case Mean age (years)
P value a
e
>0.05
>0.05
BMI (kg/m2)
Tumor locationa Case
21.2 ± 3.4 Colon cancersb GC and RC 21.5 ± 3.1 Colon cancersc GC and RC GC and DC >0.05 e
2 2 8 3 1 e
GC, gastric cancer; RC, rectal cancer; DC, duodenal cancer. b Colon cancers, containing one case of synchronous HFC (hepatic flexure colon cancer) and RC, and one case of IC (ileocecal cancer) and RC. c Colon cancers, containing 4 cases of synchronous SFC (splenic flexure colon cancer) and RC, 3 cases of HFC and RC, 1 case of IC and RC.
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hospital stay (10.0 ± 3.4 days, P > 0.05). One case of incision infection occurred postoperatively and was cured later. No postoperative mortality occurred either (Table 3) 3.3. Pathological data The specimens were confirmed by histologic diagnosis. In the open group, median numbers of lymph nodes harvested and positive were 34.3 ± 8.2 and 1.9 ± 1.5 respectively. The positive rate of lymph nodes was 5.4%. On the contrast, in laparoscopy group, the results were 39.0 ± 7.9, 3.0 ± 2.9 and 7.7% respectively. TNM stage revealed 2 cases of Stage II and 2 cases of Stage III (TNM stage was indentified according to the worse one of the multiple primary cancers) in open group. The situations in laparoscopy group were 2 cases of Stage II, 9 cases of Stage III and 1 cases of Stage IV (Table 4). 3.4. Follow-up status According to results of TNM stage, adjuvant therapy was unnecessary for 3 patients, while the other 13 patients were recommended to accept adjuvant therapy. Eleven patients underwent adjuvant therapy containing chemotherapy and radiotherapy (if necessary), while 2 patients refused adjuvant therapy. Follow-up was completed in all 16 patients for 28.7 ± 21.2 months. The results revealed 10 cases of disease free survival, 4 cases of residual disease survival and 2 cases of cancer-related death. The mortality rate was 12.5% according to the last followup result (Table 3). 4. Discussion Multiple primary cancers (MPC) can be defined as two or more different tumors synchronously or metachronously forming in the same individual. It was first described by Billroth in 1889, while its diagnostic criteria were drawn up by Warren and Gates in 1932 [5]. Then Moertel [6] categorized MPC into three groups: tumors formed in the same organ, tumors formed in different organs, and the combination of the first two cases. The incidence of MPC is low, ranging between 0.5% and 3% in China, which is much lower than that of other counties and it may be due to the unawareness and inferiority of diagnostic level [7,8]. Synchronous gastrointestinal multiple primary cancers (SGMPC) is even rare [9,10]. A prospective study revealed that 19 cases of 543 gastric cancers developed colorectal cancer synchronously [11]. Another retrospective study demonstrated 35 cases of 4426 gastric cancers developed colorectal cancer, while only 3 cases occurred synchronously [12]. In this study, the proportion of 27 cases of SGMPC in gastrointestinal primary cancers was 1.1%. These 27 cases were diagnosed by combination of gastrointestinal endoscopy and CT scan of abdomen. PET/CT was also recommended
for diagnosis of SGMPC in some cases [13]. Surgical intervention is the first option for SGMPC. However, simultaneous surgical resection indicates more difficulties and higher operation risk than surgical resection for single cancer. Take synchronous rectal and gastric cancer for example, conventional open resection requires a wide incision from xiphoid to the pubic symphysis, and may lead to a poor cosmetic result and impaired quality of postoperative life. Meanwhile, severe trauma may result in postoperative complications and a delayed recovery. Nowadays, laparoscopy surgery has been performed worldwide. Laparoscopy-assisted colorectal resection has been advocated as a standard treatment for colorectal cancer because of less trauma and faster recovery without sacrificing similar oncological outcome [14,15]. Long-term outcomes of laparoscopic distal gastrectomy for advanced gastric cancer have also been proved by some studies [16,17]. Therefore, simultaneous laparoscopy-assisted resection for SGMPC is feasible in theory. This assumption is supported by some case reports. One case of esophageal cancer with sigmoid colon cancer treated by laparoscopic surgery and another case of laparoscopic resection of sporadic synchronous gastric and jejunal gastrointestinal stromal tumors have been reported [18,19]. In addition, several cases of simultaneous laparoscopy-assisted resection for synchronous rectal and gastric cancer have been reported, and the results revealed a fast recovery, low incidence of complication and a good cosmetic result [20e22]. Experience of performing numerous laparoscopy-assisted surgeries enhanced our confidence to perform simultaneous laparoscopy-assisted resection for SGMPC. Instead of a wide incision, several small incisions were made for trocars’ placements to finish multiple tumors resection and lymphadenectomy. A median 5 cm of assisted incision was applied to remove specimen and finish digestive reconstruction. Thus, a better cosmetic result and less blood loss were guaranteed. These advantages were even significant in patients diagnosed with synchronous gastric and rectal cancer [23]. In this study, totally 5 cases of synchronous gastric and rectal cancer were included, containing 3 cases of laparoscopy surgery and 2 cases of open resection. Compared to open resection, laparoscopy-assisted combined distal gastrectomy and low anterior resection presented advantages of less blood loss (56.7 ± 25.2 vs. 200.0 ± 70.7 ml), shorter incision length (5.0 ± 0.0 vs. 19.0 ± 1.4 cm) and postoperative hospital stay (12.3 ± 2.1 vs. 17.0 ± 4.2 days). However, more cases and prospectively study, if possible, are needed to further confirm the advantages. The oncological outcomes were also discussed in our study and the results seemed satisfactory. Median number of lymph nodes harvested was equal in laparoscopy and open group. Disease free survival rate seemed better in laparoscopy group. However, due to shorter follow-up time of laparoscopy group, whether oncological outcomes of simultaneous laparoscopy-assisted resection for SGMPC is similar to the open one still need confirmation by more cases and long-term follow-up.
Table 3 Surgery data. Group
Operative methoda
Case
Operative time (min)
Blood loss (ml)
Incision length (cm)
Postoperative hospital stay (days)
Open
STCR DG þ LAR LASTCR LADG þ LALAR LADG þ LAPD e
2 2 8 3 1 e
188.8 ± 47.7
145.0 ± 75.9
16.4 ± 1.9
12.0 ± 4.8
2
228.3 ± 38.8
77.1 ± 46.3
5.2 ± 0.7
10.0 ± 3.4
1
>0.05
0.047
0.000
>0.05
Laparoscopy
P value a
Postoperative complications (case)
>0.05
STCR, sub-total colorectal resection; DG, distal gastrectomy; LAR, low anterior resection; LASTCR, Laparoscopy-assisted sub-total colorectal resection; LADG, Laparoscopyassisted distal gastrectomy; LALAR, Laparoscopy-assisted low anterior resection; LAPD, Laparoscopy-assisted pancreaticoduodenectomy.
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Table 4 Oncological outcome. Group
Open Laparoscopy P value a
Lymph nodes
TNM stage
Harvested
Positive
34.3 ± 8.2 39.0 ± 7.9 >0.05
1.9 ± 1.5 3.0 ± 2.9 >0.05
II 2 2 >0.05
Follow-up (months) III
IV
2 9
e 1
46.8 ± 29.4 23.7 ± 14.8 >0.05
Statusa DFS
RDS
CRD
2 8
1 3
1 1
DFS, Disease free survival; RDS, residual disease survival; CRD, cancer-related death.
In our experience, some key points should be paid attention to during performing simultaneous laparoscopy-assisted resection for SGMPC. First, surgeon should have plentiful experience in laparoscopy surgery. Second, surgeon should be familiar with the anatomy of gastrointestinal tract and its surrounding tissues. Third, the operator, camera surgeon and monitor should change positions timely when turning dissection of one cancer to another. Last, trocar placement should be well designed before surgery and surgeon should not hesitate to add another trocar when facing with difficult operation. Take laparoscopy-assisted combined distal gastrectomy and low anterior resection for example. When we performed laparoscopy-assisted low anterior resection first, the positions of trocars were designed nearer the head side than usual so that these trocars could be used for operation of distal gastrectomy. 5. Conclusion To our knowledge, so far our study contains maximum cases of SGMPC underwent laparoscopy surgery. SGMPC is rare and difficult to involved in cohort study, so we believe a report of 12 patients underwent laparoscopy surgery is useful even though it is a retrospective study and exist bias. Our study revealed that performed by surgeons experienced in laparoscopy surgery, laparoscopy-assisted combined resection for SGMPC is feasible, safe and effective. However, more cases and long-term follow-up are needed to confirm the surgical advantages and similar oncological outcomes. Ethical approval None. Sources of funding None. Author contribution Designed the study: Hong-bo and Jia-feng. Performed surgery: Hong-bo, Zong-heng, Jiang-long and Yong. Acquisition of data: Jiafeng and Pu-run. Analyzed the data: Bo. Wrote the paper: Jia-feng and Bo. Conflicts of interest None. Guarantor None.
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