Surg Endosc DOI 10.1007/s00464-015-4172-3
and Other Interventional Techniques
Initial experience of laparoscopic pelvic exenteration and comparison with conventional open surgery Keisuke Uehara1 • Hayato Nakamura1 • Yasushi Yoshino2 • Atsuki Arimoto1 Takehiro Kato1 • Yukihiro Yokoyama1 • Tomoki Ebata1 • Masato Nagino1
•
Received: 11 November 2014 / Accepted: 2 March 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Generalization of laparoscopic pelvic surgery has brought about profound knowledge of the pelvic anatomy and has encouraged expansion of indications for laparoscopic surgery to extended pelvic surgery. Pelvic exenteration (PE) is still a demanding surgical procedure and remains an essential technique for pelvic surgery although minimally invasive and function-preserving surgery is in the mainstream of surgical treatment. However, the techniques of laparoscopic PE (LPE) have been rarely explained nor has its feasibility been fully evaluated. The aim of this study was to describe important technical points and to assess the feasibility of LPE for pelvic malignancies. Methods Data on 67 patients with pelvic malignancies, who underwent PE between June 2006 and August 2014, were analyzed retrospectively. LPE has been indicated since 2013. Patients were divided into the LPE group (n = 9) and the conventional open PE (OPE) group (n = 58). Results Operative time in the LPE and OPE groups was similar (935 vs. 883 min, p = 0.398). Intraoperative blood loss in the LPE group was significantly less than that in the OPE group (830 vs. 2769 ml, p = 0.003). Pathological R0 resection rate was similar in both groups (77.8 vs. 75.9 %). Overall incidence of any complication and major complications were much lower in the LPE group (66.7 and 0 %)
& Keisuke Uehara [email protected] 1
Division of Surgical Oncology, Department of Surgery, Nagoya University Graduate School of Medicine, 65, Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan
2
Department of Urology, Nagoya University Graduate School of Medicine, Nagoya, Japan
compared to the OPE group (89.7 and 32.8 %), although not statistically significant (p = 0.094 and 0.053, respectively). Postoperative hospital stay was significantly shorter in the LPE group than in the OPE group (27 vs. 43 days, p = 0.003). Conclusions We confirmed that LPE for pelvic malignancies resulted in less blood loss, a lower complication rate, and shorter postoperative hospital stay compared to OPE. LPE performed by an experienced pelvic surgeon was safe and efficient, and might be a promising option for carefully selected patients. Keywords Laparoscopic surgery Pelvic exenteration Open surgery
Locally advanced or recurrent pelvic malignancies sometimes cross the frontier to easily invade adjacent organs in the narrow pelvis. Combined resection of adjacent organs and/or autonomic nervous systems may not take a patient’s life, but bring about subsequent functional impairment [1]. Although pelvic surgeons are required to achieve both curative resection with a safe margin and to preserve postoperative function, occasionally both requirements cannot be realized. To seek a cure after surgical resection, extended pelvic surgery is essential for selected patients. Pelvic exenteration (PE) provides hope when seeking curability but is still a challenging surgery and requires surgeons with ultimate surgical skills [2–4]. Laparoscopic surgery (LS) has widely and rapidly spread and has been indicated for various pelvic diseases including those of the rectum, prostate, urinary bladder, uterus, vagina, and ovary [5–9]. Indication for LS also has been expanded to locally advanced or recurrent diseases, which occasionally require extended lymph node
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dissection [10–14]. Additionally, by breaking down barriers separating specialists, laparoscopic multi-visceral resection has been attempted, and several small studies showed the feasibility of extended pelvic surgery [15–17]. Although laparoscopic PE (LPE) requires a high level of skill, technical points that should be given attention, and pitfalls of such a complicated surgical approach have not been clearly described. In addition, the safety and advantages of LPE for patients have not been fully evaluated. In our institution, PE has been aggressively performed to achieve curative resection for strictly selected patients with pelvic malignancies, and LPE was introduced in 2013. The aim of this study was to report the initial experience with LPE to discuss technical points that should be given attention and to compare the short-term results of LPE with those of conventional open PE (OPE).
are peculiar to laparoscopic procedures. Port placement for LPE was similar to that described in our previous report of laparoscopic rectal resection [22]. A total of five trocars are used as shown in Fig. 1A. Port A is a 12-mm camera port placed through the umbilical small incision. After pneumoperitoneum, two 5-mm ports and two 12-mm ports are inserted. B1 is the predeterminated site of the urostomy, and C2 is the estimated site of the colostomy. An operator mainly stands on the right side of the patient, which is similar to the position in usual laparoscopic rectal surgery, but stands on the left side when manipulating right sidewall dissection in the pelvis. At that time, the camera scope should be inserted from port C2, and the operator uses port A and B2, which results in avoiding tangential movement of surgeon’s right hand and allows for comfortable manipulation.
Patients and methods Patients Patients were selected from our prospective colorectal cancer database maintained at Nagoya University Hospital, Nagoya, Japan. Between June 2006 and August 2014, 67 consecutive patients with pelvic malignancies underwent PE with curative intent. PE was performed for (1) locally advanced rectal cancer; (2) locally recurrent rectal cancer; (3) gynecologic cancer; (4) urologic cancer; and (5) bone and soft tissue sarcoma. PE included anterior PE (APE), posterior PE (PPE), and total PE (TPE). Combined resection of the bony pelvis was performed in some patients to achieve R0 resection. Baseline assessment for resectability that included chest and abdominopelvic computed tomography and pelvic magnetic resonance imaging in all patients. All patients were selected as candidates for surgical resection at pre-treatment multi-disciplinary conferences. Contraindication for LPE included the patients with past history of multiple laparotomies, who were predicted to have severe small bowel adhesion, and the patients requiring higher or middle amputation of the sacrum [18]. In this study, patients were divided into the LPE group and OPE group, and the short-term outcomes were compared between the two groups. Surgical technique of LPE Surgical team members included colorectal and urologic surgeons. Orthopedic surgeons were included in cases requiring bony pelvic resection. Surgical procedures for conventional OPE with or without distal sacrectomy and with ischiopubic resection were previously reported [19– 21]. Here, we described technical points and pitfalls that
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Fig. 1 a Port placement of laparoscopic pelvic exenteration. A 12mm camera port; B 5-mm port; C 12-mm port. Line D indicates minilaparotomy for creating a urostomy using an ileal conduit. Operator most often stands on the right side of the patient but stands on the left side for the manipulation of the right-side pelvic wall. b Postoperative abdominal wound after total pelvic exenteration
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Surg Endosc b Fig. 2 Intraoperative photographs. A The ureter should be fully
mobilized. B The retrorectal loose connective space should be divided distally as far as possible. C Lateral dissection along to the iliac vessels (right side). D Same in the left side. E The obturator nerve should be preserved. F The dorsal vein complex is clipped and divided, and bipolar soft-coagulation performed. G The laparoscopicguided perineal approach can provide guidance for a correct dissection. H Pelvic cavity after total pelvic exenteration
Figure 2 shows representative scenes during pelvic manipulation. At the beginning of pelvic manipulation, the bilateral ureter should be confirmed and fully mobilized (Fig. 2A). The retrorectal loose connective space should be divided distally as far as possible (Fig. 2B), except in patients with the posterior type of locally recurrent rectal cancer requiring combined resection of the distal sacrum. Thereafter, bilateral pelvic side-wall dissection is performed along the internal iliac vessels (Fig. 2C, D). Several branches going toward pelvic cavity should be carefully exposed, clipped, and divided. In cases requiring combined resection of the trunk of the internal iliac vein (TIIV), the TIIV should be divided last because early division increases the pelvic venous pressure and subsequent intraoperative blood loss. The obturator nerve should be preserved bilaterally (Fig. 2E). Anterior complete mobilization causes suspension of the urinary bladder and obstructs the subsequent surgical process. Therefore, this manipulation should be performed after the completion of dissection of the posterior and bilateral side walls. The dorsal vein complex (DVC) is clipped and divided, and bipolar soft-coagulation is done using a VIO system (VIO300D; Erbe Elektromedizin, Tubingen, Germany) (Fig. 2F). Laparoscopic insertion of a urinary single-J catheter is very difficult and time consuming; therefore, the division of the ureter is conducted just before shifting to the perineal approach to avoid intraoperative urinary retention. The laparoscopic-assisted perineal approach can provide guidance for a correct dissection and avoid massive bleeding from the divided DVC just under the pubic symphysis (Fig. 2G). The specimen is extracted through the perineal wound. After closing the perineal wound, a urostomy is created by urologists through the umbilical 7-cm mini-laparotomy indicated in Line D (Fig. 1). Comparison between LPE and OPE The clinical characteristics and short-term outcomes were compared between the two groups. Short-term outcomes included operative results, such as operative time, intraoperative blood loss, urinary volume, infusion volume, fluid balance, and postoperative complications. Mortality was defined as death from any cause during the hospital
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stay or within 90 days after surgery. Postoperative complications were defined as morbidities which occurred during the hospital stay or within 30 days after surgery and recorded according to the Clavien–Dindo classification [23]. Grade 3 or higher complications were regarded as major complications. The fluid balance was calculated according to the following formula: Fluid inout balanceðml/kg/hÞ ¼ ½TIVðmlÞTBLðmlÞTUVðmlÞ=OTðhÞ=BWðkgÞ TIV: total infusion volume, TBL: total blood loss, TUV: total urinary volume, OT: operative time, BW: body weight. Statistical analysis Possible clinical characteristics and perioperative parameters were compared between the LPE and OPE group. Comparison was made by the Chi-squared test or the Mann–Whitney U test, where appropriate. A value of p \ 0.05 was considered statistically significant. Statistical analysis was done using SPSS software version 20.0 (IBM Japan Ltd., Tokyo, Japan).
Results Patients’ baseline characteristics are shown in Table 1. There were no differences in body mass index and physical status between groups. Treated diseases were similar in both groups, and neoadjuvant treatment was equivalently applied to both groups. Operative results are listed in Table 2. In the OPE group, APE and PPE were performed in three patients and one patient, respectively. The remaining 63 patients (94.0 %) in the OPE group and all patients in the LPE group underwent TPE. Combined resection of the TIIV was indicated in four patients (44.4 %) in the LPE group, which was significantly fewer than that in the OPE group (79.3 %, p = 0.04). Operative time in the LPE and OPE groups was similar (935 vs. 883 min, p = 0.398). Intraoperative blood loss was significantly less, and fluid balance was significantly lower in the LS group compared to the OS group (830 vs. 2769 ml: p = 0.003, 5.2 vs. 7.4 ml/ kg/h: p = 0.049, respectively). Pathological R0 resection rate was similar in both groups (77.8 vs. 75.9 %). Table 3 shows the postoperative courses of 84 patients. There was no mortality from postoperative complications. Overall incidence rates of any complication and major complications were much lower in the LPE group (66.7 and 0 %) than in the OPE group (89.7 and 32.8 %), although not statistically significant (p = 0.094 and 0.053,
Surg Endosc Table 1 Clinical characteristics of patients who underwent pelvic exenteration (n = 67)
Variables
Laparoscopic n=9
Open n = 58
p
Age (year), median (range)
64.0 (20–72)
60.5 (19–78)
0.905
Sex, no. (%) Male Female BMI (kg/m2), median (range)
0.434 5 (55.6)
42 (72.4)
4 (44.4)
16 (27.6)
21.5 (19.0–31.0)
21.7 (14.0–29.2)
0.672
Physical status (ASA), no. (%)
0.201
1
4 (44.4)
12 (20.7)
[2
5 (55.6)
46 (79.3) \0.001
Operative year, no. (%) 2006–2008 2009–2011 2012–2014
0
14 (24.1)
0 9 (100)
29 (50.0) 15 (25.9)
Disease, no. (%)
0.483
Primary rectal cancer
2 (22.3)
12 (20.7)
Locally recurrent rectal cancer
4 (44.4)
36 (62.1)
3(33.3)
10 (17.2)
None
3 (33.3)
19 (32.8)
Chemotherapy alone
6 (66.7)
30 (51.7)
Other diseases Neoadjuvant treatment, no. (%)
(Chemo) radiotherapy
0.423
0
9 (15.5)
BMI body mass index, ASA American Society of Anesthesiologists
Table 2 Operative results (n = 67)
Variables
Laparoscopic n=9
Open n = 58
p
Operative procedures, no (%) Anterior PE Posterior PE Total PE
0.719 0
3 (5.2)
0 9 (100)
1 (1.7) 54 (93.1)
None
6 (66.7)
22 (37.9)
With distal sacrectomy
2 (22.2)
33 (56.9)
With pubic resection
Combined resection of the bony pelvis, no (%)
0.149*
1 (11.1)
3 (5.2)
Combined resection of the TIIV, no (%)
4 (44.4)
46 (79.3)
Conversion to the open surgery, no (%)
1 (11.1)
0.040
–
–
Intraoperative parameter, median (range) Operative time (min) Blood loss (ml) Total infusion volume (ml)
935 (716–1219) 830 (283–5225) 6950 (4680–12,700)
883 (449–1552)
0.398
2769 (270–9619)
0.003
10,365 (4750–22,870)
0.010
Infusion volume (ml/kg/h)
8.9 (4.6–12.9)
12.8 (4.6–31.1)
Total urinary volume (ml)
800 (390–2050)
1155 (150–14,470)
0.151
Urinary volume (ml/kg/h)
0.7 (0.3–2.9)
1.5 (0.1–21.2)
0.064
5.2 (3.3–9.5) 7 (77.8)
7.4 (1.5–13.5) 44 (75.9)
0.049 1.000
Fluid balance (ml/kg/h) R0 resection
0.002
PE pelvic exenteration, TIIV trunk of the internal iliac vein, * None versus Yes
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Surg Endosc Table 3 Postoperative courses (n = 67)
Variables
Laparoscopic n=9
Any complication, no (%)
6 (66.7)
Anastomotic leakage
0
52 (89.7)
0.094
2 (3.5)
1.000
4 (44.4)
11 (19.0)
0.105
Urinary infection
4 (44.4)
27 (46.6)
1.000
Perineal wound infection
1 (11.1)
10 (17.2)
1.000
Pelvic sepsis
0
20 (34.5)
0.049
Small bowel perforation
0
3 (5.2)
1.000
Necrosis of ileal conduit
0
2 (3.5)
1.000
Pulmonary embolization
0
1 (1.7)
1.000
0
19 (32.8)
0.052
0 7 (4–14)
0 9 (4–62)
– 0.008
27 (23–53)
43 (19–276)
0.003
Mortality Days until oral intake (day), median (range) Postoperative hospital stay (day), median (range) [grade 3 according to the Clavien–Dindo classification
respectively). The start of oral intake was significantly earlier in the LPE group than in the OPE group (7 vs. 9 days, p = 0.003). Postoperative hospital stay was significantly shorter in the LPE group compared to the OPE group (27 vs. 43 days, p = 0.008).
Discussion PE is a maximum invasive and complicated procedure among pelvic surgeries [2–4]. As a result of early diagnosis, introduction of neoadjuvant therapy, improvement in surgical technique, avoiding extended surgery and preserving the function of adjacent organs as far as possible are currently in the mainstream of treatment of pelvic malignancies. However, PE remains an essential surgical procedure for some patients with highly advanced or recurrent pelvic malignancies. On the other hand, the excellent magnified view provided by LS has encouraged pelvic surgeons to indicate LS for PE [16, 17]. In this study, we showed that LPE for pelvic malignancies provided safety with less blood loss, a lower complication rate, and shorter postoperative hospital stay, compared with OPE. Although the technical aspects of conventional OPE have been reported previously [18–21], those of LPE have been rarely shown [17, 24]. In this article, we described the technical points and pitfalls that were peculiar to laparoscopic procedures. We emphasized strongly that posterior and side-wall dissection should be performed in the earlier period in the pelvic phase and distally as far as possible, and anterior dissection should be performed in the last phase, as suspension of the urinary bladder obstructs subsequent surgical maneuvers. Meticulous transection of small brunches of the venous network in the pelvis was a key to avoid intraoperative bleeding in LPE; therefore,
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p
Ileus
Major complications, no (%)a
a
Open n = 58
dissection along to the internal iliac vessels is essential. The laparoscopic-guided perineal approach helped us to achieve a proper dissection, which avoided much blood loss during the approach. PE is a common name for the procedure that includes heterogeneous types of multi-visceral resection. The extent of resection varies according to the site and extension of the disease. Factors predicting the difficulty of PE include combined resection of the TIIV and/or bony pelvis. Although previous studies indicated that LS prolonged operative time significantly compared to conventional open surgery [22, 25–27], operative time in this study was similar in both LPE and OPE groups. The reason might be that the rates of combined resection of both bony pelvis and TIIV were significantly lower in the LES group than in the OPE group. That means that in this series, PE requiring a high level of technical expertise was less frequently performed in the LPE group. We suggested that LPE with a low level of difficulty was a promising option in PE. We experienced a case with conversion to OPE. This case had previous history of rectal prolapse and underwent open rectopexy using mesh. Locally advanced rectal cancer caused a pelvic abscess, and the pelvic space became ill-defined and as hard as rock by the infected mesh, making accomplishment of LS impossible. Patients with expectations of an ill-defined pelvic anatomy are not likely to be suitable for LPE. Although appropriate indications for LPE should be discussed in the future, indication for laparoscopic rectal surgery has been gradually expanded, and we expect that higher-skilled pelvic surgery becomes safely possible by our improving skill. In this study, a single surgeon performed LPE in all cases and OPE in 51 cases (87.9 %). Although our study showed that an experienced surgeon could perform LPE safely in the carefully selected patients, the small number of patients in this retrospective study was a major
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limitation. Moreover, also that LPE was performed in the last 2 years of the study period could have biased the results. Our results showed that LS achieved a similar rate of pathological R0 resection compared to OS. However, a further prospective observational study to evaluate not only the short-term but also long-term outcome is needed.
Conclusions Details of technical points and pitfalls of LPE were described. We confirmed that LPE for pelvic malignancies resulted in less blood loss, a lower complication rate, and shorter postoperative hospital stay compared to OPE. LPE performed by an experienced pelvic surgeon was safe and efficient and might be a promising option for carefully selected patients. Disclosures Keisuke Uehara, Hayato Nakamura, Yasushi Yoshino, Atsuki Arimoto, Takehiro Kato1, Yukihiro Yokoyama, Tomoki Ebata, and Masato Nagino have no conflicts of interest or financial ties to disclose.
References 1. Rezk YA, Hurley KE, Carter J et al (2013) A prospective study of quality of life in patients undergoing pelvic exenteration: interim results. Gynecol Oncol 128:191–197 2. Vermaas M, Ferenschild FT, Verhoef C et al (2007) Total pelvic exenteration for primary locally advanced and locally recurrent rectal cancer. Eur J Surg Oncol 33:452–458 3. Chiantera V, Rossi M, De Iaco P et al (2014) Morbidity after pelvic exenteration for gynecological malignancies: a retrospective multicentric study of 230 patients. Int J Gynecol Cancer 24:156–164 4. Speicher PJ, Turley RS, Sloane JL et al (2014) Pelvic exenteration for the treatment of locally advanced colorectal and bladder malignancies in the modern era. J Gastrointest Surg 18:782–788 5. Jayne DG, Thorpe HC, Copeland J et al (2010) Five-year followup of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97:1638–1645 6. van der Pas MH, Haglind E, Cuesta MA et al (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218 7. Jeong SY, Park JW, Nam BH et al (2014) Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol 15:767–774 8. Porpiglia F, Renard J, Billia M et al (2007) Open versus laparoscopy-assisted radical cystectomy: results of a prospective study. J Endourol 21:325–329 9. Vizza E, Pellegrino A, Milani R et al (2011) Total laparoscopic radical hysterectomy and pelvic lymphadenectomy in locally advanced stage IB2-IIB cervical cancer patients after neoadjuvant chemotherapy. Eur J Surg Oncol 37:364–369
10. Konishi T, Kuroyanagi H, Oya M et al (2011) Multimedia article. Lateral lymph node dissection with preoperative chemoradiation for locally advanced lower rectal cancer through a laparoscopic approach. Surg Endosc 25:2358–2359 11. Park JS, Choi GS, Lim KH et al (2011) Laparoscopic extended lateral pelvic node dissection following total mesorectal excision for advanced rectal cancer: initial clinical experience. Surg Endosc 25:3322–3329 12. Liang JT (2011) Technical feasibility of laparoscopic lateral pelvic lymph node dissection for patients with low rectal cancer after concurrent chemoradiation therapy. Ann Surg Oncol 18:153–159 13. Di Benedetto A, Soares R, Dovey Z et al (2014) Laparoscopic radical prostatectomy for high-risk prostate cancer. BJU Int (Epub ahead of print) 14. Del Pino M, Fuste´ P, Pahisa J et al (2013) Laparoscopic lymphadenectomy in advanced cervical cancer: prognostic and therapeutic value. Int J Gynecol Cancer 23:1675–1683 ´ lvarez E 15. Ferna´ndez-Martı´nez D, Rodrı´guez-Infante A, Castelo-A et al (2014) Combined radical prostatectomy and abdominoperineal resection for locally invasive rectal cancer. Int J Surg Case Rep 5:584–588 16. Martı´nez A, Filleron T, Vitse L et al (2011) Laparoscopic pelvic exenteration for gynaecological malignancy: Is there any advantage? Gynecol Oncol 120:374–379 17. Mukai T, Akiyoshi T, Ueno M et al (2013) Laparoscopic total pelvic exenteration with en bloc lateral lymph node dissection after neoadjuvant chemoradiotherapy for advanced primary rectal cancer. Asian J Endosc Surg 6:314–317 18. Uehara K, Ito Z, Yoshino Y et al (2014) Aggressive surgical treatment with bony pelvic resectionfor locally recurrent rectal cancer. Eur J Surg Oncol (Epub ahead of print) 19. Moriya Y, Isgiguro S (2013) Pelvic exenteration: total/anterior/posterior. In: Khatri VP (ed) Atlas of advanced operative surgery. Elsevier Publishers, Philadelphia, pp 438–446 20. Moriya Y, Uehara K (2013) Total pelvic exenteration with distal sacrectomy for fixed locally recurrent rectal cancer. In: Khatri VP (ed) Atlas of advanced operative surgery. Elsevier Publishers, Philadelphia, pp 430–437 21. Uehara K, Yoshioka Y, Taguchi Y et al (2012) Locally recurrent rectal cancer successfully treated by total pelvic exenteration with combined ischiopubic rami resection: report of a case. Jpn J Clin Oncol 42:58–62 22. Uehara K, Yamamoto S, Fujita S, Akasu T, Moriya Y (2006) Surgical outcomes of laparoscopic versus open surgery for rectal carcinoma—a matched case–control study. Hepatogastroenterology 53:531–535 23. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213 24. Ferron G, Querleu D, Martel P, Letourneur B, Soulie´ M (2006) Laparoscopy-assisted vaginal pelvic exenteration. Gynecol Oncol 100:551–555 25. Veldkamp R, Kuhry E, Hop WC (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6:477–484 26. Guillou PJ, Quirke P, Thorpe H et al (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 365:1718–1726 27. Yamamoto S, Inomata M, Katayama H et al (2014) Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg 260:23–30
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and Other Interventional Techniques
Initial experience of laparoscopic pelvic exenteration and comparison with conventional open surgery Keisuke Uehara1 • Hayato Nakamura1 • Yasushi Yoshino2 • Atsuki Arimoto1 Takehiro Kato1 • Yukihiro Yokoyama1 • Tomoki Ebata1 • Masato Nagino1
•
Received: 11 November 2014 / Accepted: 2 March 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Generalization of laparoscopic pelvic surgery has brought about profound knowledge of the pelvic anatomy and has encouraged expansion of indications for laparoscopic surgery to extended pelvic surgery. Pelvic exenteration (PE) is still a demanding surgical procedure and remains an essential technique for pelvic surgery although minimally invasive and function-preserving surgery is in the mainstream of surgical treatment. However, the techniques of laparoscopic PE (LPE) have been rarely explained nor has its feasibility been fully evaluated. The aim of this study was to describe important technical points and to assess the feasibility of LPE for pelvic malignancies. Methods Data on 67 patients with pelvic malignancies, who underwent PE between June 2006 and August 2014, were analyzed retrospectively. LPE has been indicated since 2013. Patients were divided into the LPE group (n = 9) and the conventional open PE (OPE) group (n = 58). Results Operative time in the LPE and OPE groups was similar (935 vs. 883 min, p = 0.398). Intraoperative blood loss in the LPE group was significantly less than that in the OPE group (830 vs. 2769 ml, p = 0.003). Pathological R0 resection rate was similar in both groups (77.8 vs. 75.9 %). Overall incidence of any complication and major complications were much lower in the LPE group (66.7 and 0 %)
& Keisuke Uehara [email protected] 1
Division of Surgical Oncology, Department of Surgery, Nagoya University Graduate School of Medicine, 65, Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan
2
Department of Urology, Nagoya University Graduate School of Medicine, Nagoya, Japan
compared to the OPE group (89.7 and 32.8 %), although not statistically significant (p = 0.094 and 0.053, respectively). Postoperative hospital stay was significantly shorter in the LPE group than in the OPE group (27 vs. 43 days, p = 0.003). Conclusions We confirmed that LPE for pelvic malignancies resulted in less blood loss, a lower complication rate, and shorter postoperative hospital stay compared to OPE. LPE performed by an experienced pelvic surgeon was safe and efficient, and might be a promising option for carefully selected patients. Keywords Laparoscopic surgery Pelvic exenteration Open surgery
Locally advanced or recurrent pelvic malignancies sometimes cross the frontier to easily invade adjacent organs in the narrow pelvis. Combined resection of adjacent organs and/or autonomic nervous systems may not take a patient’s life, but bring about subsequent functional impairment [1]. Although pelvic surgeons are required to achieve both curative resection with a safe margin and to preserve postoperative function, occasionally both requirements cannot be realized. To seek a cure after surgical resection, extended pelvic surgery is essential for selected patients. Pelvic exenteration (PE) provides hope when seeking curability but is still a challenging surgery and requires surgeons with ultimate surgical skills [2–4]. Laparoscopic surgery (LS) has widely and rapidly spread and has been indicated for various pelvic diseases including those of the rectum, prostate, urinary bladder, uterus, vagina, and ovary [5–9]. Indication for LS also has been expanded to locally advanced or recurrent diseases, which occasionally require extended lymph node
123
Surg Endosc
dissection [10–14]. Additionally, by breaking down barriers separating specialists, laparoscopic multi-visceral resection has been attempted, and several small studies showed the feasibility of extended pelvic surgery [15–17]. Although laparoscopic PE (LPE) requires a high level of skill, technical points that should be given attention, and pitfalls of such a complicated surgical approach have not been clearly described. In addition, the safety and advantages of LPE for patients have not been fully evaluated. In our institution, PE has been aggressively performed to achieve curative resection for strictly selected patients with pelvic malignancies, and LPE was introduced in 2013. The aim of this study was to report the initial experience with LPE to discuss technical points that should be given attention and to compare the short-term results of LPE with those of conventional open PE (OPE).
are peculiar to laparoscopic procedures. Port placement for LPE was similar to that described in our previous report of laparoscopic rectal resection [22]. A total of five trocars are used as shown in Fig. 1A. Port A is a 12-mm camera port placed through the umbilical small incision. After pneumoperitoneum, two 5-mm ports and two 12-mm ports are inserted. B1 is the predeterminated site of the urostomy, and C2 is the estimated site of the colostomy. An operator mainly stands on the right side of the patient, which is similar to the position in usual laparoscopic rectal surgery, but stands on the left side when manipulating right sidewall dissection in the pelvis. At that time, the camera scope should be inserted from port C2, and the operator uses port A and B2, which results in avoiding tangential movement of surgeon’s right hand and allows for comfortable manipulation.
Patients and methods Patients Patients were selected from our prospective colorectal cancer database maintained at Nagoya University Hospital, Nagoya, Japan. Between June 2006 and August 2014, 67 consecutive patients with pelvic malignancies underwent PE with curative intent. PE was performed for (1) locally advanced rectal cancer; (2) locally recurrent rectal cancer; (3) gynecologic cancer; (4) urologic cancer; and (5) bone and soft tissue sarcoma. PE included anterior PE (APE), posterior PE (PPE), and total PE (TPE). Combined resection of the bony pelvis was performed in some patients to achieve R0 resection. Baseline assessment for resectability that included chest and abdominopelvic computed tomography and pelvic magnetic resonance imaging in all patients. All patients were selected as candidates for surgical resection at pre-treatment multi-disciplinary conferences. Contraindication for LPE included the patients with past history of multiple laparotomies, who were predicted to have severe small bowel adhesion, and the patients requiring higher or middle amputation of the sacrum [18]. In this study, patients were divided into the LPE group and OPE group, and the short-term outcomes were compared between the two groups. Surgical technique of LPE Surgical team members included colorectal and urologic surgeons. Orthopedic surgeons were included in cases requiring bony pelvic resection. Surgical procedures for conventional OPE with or without distal sacrectomy and with ischiopubic resection were previously reported [19– 21]. Here, we described technical points and pitfalls that
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Fig. 1 a Port placement of laparoscopic pelvic exenteration. A 12mm camera port; B 5-mm port; C 12-mm port. Line D indicates minilaparotomy for creating a urostomy using an ileal conduit. Operator most often stands on the right side of the patient but stands on the left side for the manipulation of the right-side pelvic wall. b Postoperative abdominal wound after total pelvic exenteration
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Surg Endosc b Fig. 2 Intraoperative photographs. A The ureter should be fully
mobilized. B The retrorectal loose connective space should be divided distally as far as possible. C Lateral dissection along to the iliac vessels (right side). D Same in the left side. E The obturator nerve should be preserved. F The dorsal vein complex is clipped and divided, and bipolar soft-coagulation performed. G The laparoscopicguided perineal approach can provide guidance for a correct dissection. H Pelvic cavity after total pelvic exenteration
Figure 2 shows representative scenes during pelvic manipulation. At the beginning of pelvic manipulation, the bilateral ureter should be confirmed and fully mobilized (Fig. 2A). The retrorectal loose connective space should be divided distally as far as possible (Fig. 2B), except in patients with the posterior type of locally recurrent rectal cancer requiring combined resection of the distal sacrum. Thereafter, bilateral pelvic side-wall dissection is performed along the internal iliac vessels (Fig. 2C, D). Several branches going toward pelvic cavity should be carefully exposed, clipped, and divided. In cases requiring combined resection of the trunk of the internal iliac vein (TIIV), the TIIV should be divided last because early division increases the pelvic venous pressure and subsequent intraoperative blood loss. The obturator nerve should be preserved bilaterally (Fig. 2E). Anterior complete mobilization causes suspension of the urinary bladder and obstructs the subsequent surgical process. Therefore, this manipulation should be performed after the completion of dissection of the posterior and bilateral side walls. The dorsal vein complex (DVC) is clipped and divided, and bipolar soft-coagulation is done using a VIO system (VIO300D; Erbe Elektromedizin, Tubingen, Germany) (Fig. 2F). Laparoscopic insertion of a urinary single-J catheter is very difficult and time consuming; therefore, the division of the ureter is conducted just before shifting to the perineal approach to avoid intraoperative urinary retention. The laparoscopic-assisted perineal approach can provide guidance for a correct dissection and avoid massive bleeding from the divided DVC just under the pubic symphysis (Fig. 2G). The specimen is extracted through the perineal wound. After closing the perineal wound, a urostomy is created by urologists through the umbilical 7-cm mini-laparotomy indicated in Line D (Fig. 1). Comparison between LPE and OPE The clinical characteristics and short-term outcomes were compared between the two groups. Short-term outcomes included operative results, such as operative time, intraoperative blood loss, urinary volume, infusion volume, fluid balance, and postoperative complications. Mortality was defined as death from any cause during the hospital
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stay or within 90 days after surgery. Postoperative complications were defined as morbidities which occurred during the hospital stay or within 30 days after surgery and recorded according to the Clavien–Dindo classification [23]. Grade 3 or higher complications were regarded as major complications. The fluid balance was calculated according to the following formula: Fluid inout balanceðml/kg/hÞ ¼ ½TIVðmlÞTBLðmlÞTUVðmlÞ=OTðhÞ=BWðkgÞ TIV: total infusion volume, TBL: total blood loss, TUV: total urinary volume, OT: operative time, BW: body weight. Statistical analysis Possible clinical characteristics and perioperative parameters were compared between the LPE and OPE group. Comparison was made by the Chi-squared test or the Mann–Whitney U test, where appropriate. A value of p \ 0.05 was considered statistically significant. Statistical analysis was done using SPSS software version 20.0 (IBM Japan Ltd., Tokyo, Japan).
Results Patients’ baseline characteristics are shown in Table 1. There were no differences in body mass index and physical status between groups. Treated diseases were similar in both groups, and neoadjuvant treatment was equivalently applied to both groups. Operative results are listed in Table 2. In the OPE group, APE and PPE were performed in three patients and one patient, respectively. The remaining 63 patients (94.0 %) in the OPE group and all patients in the LPE group underwent TPE. Combined resection of the TIIV was indicated in four patients (44.4 %) in the LPE group, which was significantly fewer than that in the OPE group (79.3 %, p = 0.04). Operative time in the LPE and OPE groups was similar (935 vs. 883 min, p = 0.398). Intraoperative blood loss was significantly less, and fluid balance was significantly lower in the LS group compared to the OS group (830 vs. 2769 ml: p = 0.003, 5.2 vs. 7.4 ml/ kg/h: p = 0.049, respectively). Pathological R0 resection rate was similar in both groups (77.8 vs. 75.9 %). Table 3 shows the postoperative courses of 84 patients. There was no mortality from postoperative complications. Overall incidence rates of any complication and major complications were much lower in the LPE group (66.7 and 0 %) than in the OPE group (89.7 and 32.8 %), although not statistically significant (p = 0.094 and 0.053,
Surg Endosc Table 1 Clinical characteristics of patients who underwent pelvic exenteration (n = 67)
Variables
Laparoscopic n=9
Open n = 58
p
Age (year), median (range)
64.0 (20–72)
60.5 (19–78)
0.905
Sex, no. (%) Male Female BMI (kg/m2), median (range)
0.434 5 (55.6)
42 (72.4)
4 (44.4)
16 (27.6)
21.5 (19.0–31.0)
21.7 (14.0–29.2)
0.672
Physical status (ASA), no. (%)
0.201
1
4 (44.4)
12 (20.7)
[2
5 (55.6)
46 (79.3) \0.001
Operative year, no. (%) 2006–2008 2009–2011 2012–2014
0
14 (24.1)
0 9 (100)
29 (50.0) 15 (25.9)
Disease, no. (%)
0.483
Primary rectal cancer
2 (22.3)
12 (20.7)
Locally recurrent rectal cancer
4 (44.4)
36 (62.1)
3(33.3)
10 (17.2)
None
3 (33.3)
19 (32.8)
Chemotherapy alone
6 (66.7)
30 (51.7)
Other diseases Neoadjuvant treatment, no. (%)
(Chemo) radiotherapy
0.423
0
9 (15.5)
BMI body mass index, ASA American Society of Anesthesiologists
Table 2 Operative results (n = 67)
Variables
Laparoscopic n=9
Open n = 58
p
Operative procedures, no (%) Anterior PE Posterior PE Total PE
0.719 0
3 (5.2)
0 9 (100)
1 (1.7) 54 (93.1)
None
6 (66.7)
22 (37.9)
With distal sacrectomy
2 (22.2)
33 (56.9)
With pubic resection
Combined resection of the bony pelvis, no (%)
0.149*
1 (11.1)
3 (5.2)
Combined resection of the TIIV, no (%)
4 (44.4)
46 (79.3)
Conversion to the open surgery, no (%)
1 (11.1)
0.040
–
–
Intraoperative parameter, median (range) Operative time (min) Blood loss (ml) Total infusion volume (ml)
935 (716–1219) 830 (283–5225) 6950 (4680–12,700)
883 (449–1552)
0.398
2769 (270–9619)
0.003
10,365 (4750–22,870)
0.010
Infusion volume (ml/kg/h)
8.9 (4.6–12.9)
12.8 (4.6–31.1)
Total urinary volume (ml)
800 (390–2050)
1155 (150–14,470)
0.151
Urinary volume (ml/kg/h)
0.7 (0.3–2.9)
1.5 (0.1–21.2)
0.064
5.2 (3.3–9.5) 7 (77.8)
7.4 (1.5–13.5) 44 (75.9)
0.049 1.000
Fluid balance (ml/kg/h) R0 resection
0.002
PE pelvic exenteration, TIIV trunk of the internal iliac vein, * None versus Yes
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Surg Endosc Table 3 Postoperative courses (n = 67)
Variables
Laparoscopic n=9
Any complication, no (%)
6 (66.7)
Anastomotic leakage
0
52 (89.7)
0.094
2 (3.5)
1.000
4 (44.4)
11 (19.0)
0.105
Urinary infection
4 (44.4)
27 (46.6)
1.000
Perineal wound infection
1 (11.1)
10 (17.2)
1.000
Pelvic sepsis
0
20 (34.5)
0.049
Small bowel perforation
0
3 (5.2)
1.000
Necrosis of ileal conduit
0
2 (3.5)
1.000
Pulmonary embolization
0
1 (1.7)
1.000
0
19 (32.8)
0.052
0 7 (4–14)
0 9 (4–62)
– 0.008
27 (23–53)
43 (19–276)
0.003
Mortality Days until oral intake (day), median (range) Postoperative hospital stay (day), median (range) [grade 3 according to the Clavien–Dindo classification
respectively). The start of oral intake was significantly earlier in the LPE group than in the OPE group (7 vs. 9 days, p = 0.003). Postoperative hospital stay was significantly shorter in the LPE group compared to the OPE group (27 vs. 43 days, p = 0.008).
Discussion PE is a maximum invasive and complicated procedure among pelvic surgeries [2–4]. As a result of early diagnosis, introduction of neoadjuvant therapy, improvement in surgical technique, avoiding extended surgery and preserving the function of adjacent organs as far as possible are currently in the mainstream of treatment of pelvic malignancies. However, PE remains an essential surgical procedure for some patients with highly advanced or recurrent pelvic malignancies. On the other hand, the excellent magnified view provided by LS has encouraged pelvic surgeons to indicate LS for PE [16, 17]. In this study, we showed that LPE for pelvic malignancies provided safety with less blood loss, a lower complication rate, and shorter postoperative hospital stay, compared with OPE. Although the technical aspects of conventional OPE have been reported previously [18–21], those of LPE have been rarely shown [17, 24]. In this article, we described the technical points and pitfalls that were peculiar to laparoscopic procedures. We emphasized strongly that posterior and side-wall dissection should be performed in the earlier period in the pelvic phase and distally as far as possible, and anterior dissection should be performed in the last phase, as suspension of the urinary bladder obstructs subsequent surgical maneuvers. Meticulous transection of small brunches of the venous network in the pelvis was a key to avoid intraoperative bleeding in LPE; therefore,
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p
Ileus
Major complications, no (%)a
a
Open n = 58
dissection along to the internal iliac vessels is essential. The laparoscopic-guided perineal approach helped us to achieve a proper dissection, which avoided much blood loss during the approach. PE is a common name for the procedure that includes heterogeneous types of multi-visceral resection. The extent of resection varies according to the site and extension of the disease. Factors predicting the difficulty of PE include combined resection of the TIIV and/or bony pelvis. Although previous studies indicated that LS prolonged operative time significantly compared to conventional open surgery [22, 25–27], operative time in this study was similar in both LPE and OPE groups. The reason might be that the rates of combined resection of both bony pelvis and TIIV were significantly lower in the LES group than in the OPE group. That means that in this series, PE requiring a high level of technical expertise was less frequently performed in the LPE group. We suggested that LPE with a low level of difficulty was a promising option in PE. We experienced a case with conversion to OPE. This case had previous history of rectal prolapse and underwent open rectopexy using mesh. Locally advanced rectal cancer caused a pelvic abscess, and the pelvic space became ill-defined and as hard as rock by the infected mesh, making accomplishment of LS impossible. Patients with expectations of an ill-defined pelvic anatomy are not likely to be suitable for LPE. Although appropriate indications for LPE should be discussed in the future, indication for laparoscopic rectal surgery has been gradually expanded, and we expect that higher-skilled pelvic surgery becomes safely possible by our improving skill. In this study, a single surgeon performed LPE in all cases and OPE in 51 cases (87.9 %). Although our study showed that an experienced surgeon could perform LPE safely in the carefully selected patients, the small number of patients in this retrospective study was a major
Surg Endosc
limitation. Moreover, also that LPE was performed in the last 2 years of the study period could have biased the results. Our results showed that LS achieved a similar rate of pathological R0 resection compared to OS. However, a further prospective observational study to evaluate not only the short-term but also long-term outcome is needed.
Conclusions Details of technical points and pitfalls of LPE were described. We confirmed that LPE for pelvic malignancies resulted in less blood loss, a lower complication rate, and shorter postoperative hospital stay compared to OPE. LPE performed by an experienced pelvic surgeon was safe and efficient and might be a promising option for carefully selected patients. Disclosures Keisuke Uehara, Hayato Nakamura, Yasushi Yoshino, Atsuki Arimoto, Takehiro Kato1, Yukihiro Yokoyama, Tomoki Ebata, and Masato Nagino have no conflicts of interest or financial ties to disclose.
References 1. Rezk YA, Hurley KE, Carter J et al (2013) A prospective study of quality of life in patients undergoing pelvic exenteration: interim results. Gynecol Oncol 128:191–197 2. Vermaas M, Ferenschild FT, Verhoef C et al (2007) Total pelvic exenteration for primary locally advanced and locally recurrent rectal cancer. Eur J Surg Oncol 33:452–458 3. Chiantera V, Rossi M, De Iaco P et al (2014) Morbidity after pelvic exenteration for gynecological malignancies: a retrospective multicentric study of 230 patients. Int J Gynecol Cancer 24:156–164 4. Speicher PJ, Turley RS, Sloane JL et al (2014) Pelvic exenteration for the treatment of locally advanced colorectal and bladder malignancies in the modern era. J Gastrointest Surg 18:782–788 5. Jayne DG, Thorpe HC, Copeland J et al (2010) Five-year followup of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97:1638–1645 6. van der Pas MH, Haglind E, Cuesta MA et al (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218 7. Jeong SY, Park JW, Nam BH et al (2014) Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol 15:767–774 8. Porpiglia F, Renard J, Billia M et al (2007) Open versus laparoscopy-assisted radical cystectomy: results of a prospective study. J Endourol 21:325–329 9. Vizza E, Pellegrino A, Milani R et al (2011) Total laparoscopic radical hysterectomy and pelvic lymphadenectomy in locally advanced stage IB2-IIB cervical cancer patients after neoadjuvant chemotherapy. Eur J Surg Oncol 37:364–369
10. Konishi T, Kuroyanagi H, Oya M et al (2011) Multimedia article. Lateral lymph node dissection with preoperative chemoradiation for locally advanced lower rectal cancer through a laparoscopic approach. Surg Endosc 25:2358–2359 11. Park JS, Choi GS, Lim KH et al (2011) Laparoscopic extended lateral pelvic node dissection following total mesorectal excision for advanced rectal cancer: initial clinical experience. Surg Endosc 25:3322–3329 12. Liang JT (2011) Technical feasibility of laparoscopic lateral pelvic lymph node dissection for patients with low rectal cancer after concurrent chemoradiation therapy. Ann Surg Oncol 18:153–159 13. Di Benedetto A, Soares R, Dovey Z et al (2014) Laparoscopic radical prostatectomy for high-risk prostate cancer. BJU Int (Epub ahead of print) 14. Del Pino M, Fuste´ P, Pahisa J et al (2013) Laparoscopic lymphadenectomy in advanced cervical cancer: prognostic and therapeutic value. Int J Gynecol Cancer 23:1675–1683 ´ lvarez E 15. Ferna´ndez-Martı´nez D, Rodrı´guez-Infante A, Castelo-A et al (2014) Combined radical prostatectomy and abdominoperineal resection for locally invasive rectal cancer. Int J Surg Case Rep 5:584–588 16. Martı´nez A, Filleron T, Vitse L et al (2011) Laparoscopic pelvic exenteration for gynaecological malignancy: Is there any advantage? Gynecol Oncol 120:374–379 17. Mukai T, Akiyoshi T, Ueno M et al (2013) Laparoscopic total pelvic exenteration with en bloc lateral lymph node dissection after neoadjuvant chemoradiotherapy for advanced primary rectal cancer. Asian J Endosc Surg 6:314–317 18. Uehara K, Ito Z, Yoshino Y et al (2014) Aggressive surgical treatment with bony pelvic resectionfor locally recurrent rectal cancer. Eur J Surg Oncol (Epub ahead of print) 19. Moriya Y, Isgiguro S (2013) Pelvic exenteration: total/anterior/posterior. In: Khatri VP (ed) Atlas of advanced operative surgery. Elsevier Publishers, Philadelphia, pp 438–446 20. Moriya Y, Uehara K (2013) Total pelvic exenteration with distal sacrectomy for fixed locally recurrent rectal cancer. In: Khatri VP (ed) Atlas of advanced operative surgery. Elsevier Publishers, Philadelphia, pp 430–437 21. Uehara K, Yoshioka Y, Taguchi Y et al (2012) Locally recurrent rectal cancer successfully treated by total pelvic exenteration with combined ischiopubic rami resection: report of a case. Jpn J Clin Oncol 42:58–62 22. Uehara K, Yamamoto S, Fujita S, Akasu T, Moriya Y (2006) Surgical outcomes of laparoscopic versus open surgery for rectal carcinoma—a matched case–control study. Hepatogastroenterology 53:531–535 23. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213 24. Ferron G, Querleu D, Martel P, Letourneur B, Soulie´ M (2006) Laparoscopy-assisted vaginal pelvic exenteration. Gynecol Oncol 100:551–555 25. Veldkamp R, Kuhry E, Hop WC (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6:477–484 26. Guillou PJ, Quirke P, Thorpe H et al (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 365:1718–1726 27. Yamamoto S, Inomata M, Katayama H et al (2014) Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg 260:23–30
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