Surg Today DOI 10.1007/s00595-014-1021-2

Review Article

Laparoscopic distal pancreatosplenectomy for pancreatic ductal adenocarcinoma Tamotsu Kuroki · Susumu Eguchi 

Received: 2 August 2014 / Accepted: 10 August 2014 © Springer Japan 2014

Abstract Laparoscopic distal pancreatectomy (LDP) including laparoscopic distal pancreatosplenectomy has rapidly developed as a minimally invasive surgery. LDP is mainly indicated for benign disease and low-grade malignancy during the initial period. In recent years, an increasing number of LDPs for pancreatic ductal adenocarcinoma (PDAC) have been reported. However, the benefits of LPD for PDAC, especially in view of the oncological benefits, are unclear and remain controversial. In this review of the literature, we note that LDP has been found to be a technically feasible and safe surgical procedure in selected patients and that LDP has the advantages expected of a minimally invasive surgery. In addition, LDP has oncological feasibility for PDAC in light of its favorable rate of R0 resection and lymph node harvest compared to conventional laparotomy. Large randomized and controlled prospective studies are needed to determine the clinical advantages of LDP for left-sided PDAC.

laparoscopic distal pancreatectomy (LDP) was reported in 1996 [1]. Subsequently, the development of endoscopic instruments and improvements of minimally invasive surgical techniques have allowed for LDP [including laparoscopic distal pancreatosplenectomy (LDPS) and laparoscopic distal pancreatectomy with splenic preservation] to gain worldwide acceptance as a choice of treatment for benign pancreatic diseases and low-grade malignancies in the body and tail of the pancreas [2–13]. The benefits of LDP for pancreatic ductal adenocarcinoma (PDAC) are less clear. Few studies have described LDP as an acceptable approach for the resection of PDAC of the left-sided pancreas in selected patients [14–21]. However, to the best of our knowledge, no well-designed study comparing LDP to conventional open distal pancreatectomy has been published. This review focuses on the surgical techniques and practical benefits of LDP, and we discuss the existing problems and future prospects of LDP for PDAC.

Keywords Laparoscopic · Distal pancreatosplenectomy · Pancreatic adenocarcinoma · Minimally invasive surgery Surgical technique Introduction Laparoscopic surgery provides clear advantages compared to conventional open surgery, including less intraoperative blood loss, less postoperative pain, a shorter hospital stay and a better cosmetic outcome; and thus, laparoscopic surgery has been adopted for many organs. The first T. Kuroki (*) · S. Eguchi  Department of Surgery, Graduate School of Biomedical Sciences, Nagasaki University, 1‑7‑1 Sakamoto, Nagasaki 852‑8501, Japan e-mail: tkuroki‑[email protected]

Distal pancreatosplenectomy (DPS) with systemic lymphadenectomy is the standard surgical procedure for PDAC. In addition, a margin-negative pancreatectomy is necessary to provide a curative resection and ensure a positive long-term outcome. Moreover, a surgical strategy using early vascular control and no-touch isolation with en bloc resection is important for the oncological cure. Strasberg et al. [22] proposed a radical antegrade modular pancreatosplenectomy (RAMPS) to eliminate these problems associated with the surgical treatment of left-sided PDAC. In a RAMPS, the dissection with lymphadenectomy proceeds from right to left after the division of the pancreatic

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parenchyma, splenic artery and splenic vein. A RAMPS is conducted properly as an anterior RAMPS or posterior RAMPS, depending on the extent of penetration of the tumor. The anterior RAMPS and posterior RAMPS are distinguished by findings above or below the plane of the posterior dissection to the left adrenal gland and Gerota’s fascia. The concept of the surgical strategy for the LDPS for PDAC is the same as that of open distal pancreatosplenectomy (ODPS). The most important point of the oncological concept for PDAC is that tumors with regional lymph nodes are taken en bloc to avoid leaving behind any residual tumor. Thus, several reports have described that RAMPS is recommended as the standard LDPS technique for PDAC [23–25]. Laparoscopic approaches using a magnified view have a potential advantage in that they can provide improved visualization of the anatomy for the resection of complex vessels or lymphadenectomy along appropriate planes for the RAMPS. In addition, laparoscopic surgery has the advantage of giving a unique view from the caudal side for the safe and clear dissection of the PDAC in the body and tail of the pancreas with regional lymph nodes, from the precise plane for the RAMPS. However, Marangos et al. [17] proposed that the dissection planes for the conventional left-to-right technique of the LDPS could be chosen based on the laparoscopic visualization of the relevant anatomy, combined with intraoperative laparoscopic ultrasonography, and lymphadenectomy was performed only for enlarged or suspicious local lymph nodes. Locally advanced PDAC of the pancreatic body often involves the common hepatic artery and/or celiac axis, with perineural invasion in the nerve plexus surrounding these arteries. Hirano et al. [26] reported that distal pancreatectomy with en bloc celiac axis resection (DP-CAR) for locally advanced PDAC of the pancreatic body is feasible and safe and that it has the potential to achieve complete local control. Cho et al. [27] described that laparoscopic DP-CAR is minimally invasive, safe and feasible and can achieve R0 resection in selected patients with locally advanced PDAC. However, the benefits and feasibility of DP-CAR using the laparoscopic approach are not yet clear. Laparoscopic DP-CAR is a technically challenging operation that must be performed by expert laparoscopic surgeons and requires an advanced degree of laparoscopic skills.

Perioperative outcomes The main published series of LDPS for PDAC are listed in Table  1. Pancreatic fistula formation is the most problematic complication of DP after both open and laparoscopic

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procedures. Several reports have described that the rates of pancreatic fistula formation in LDP cases are similar to those in open distal pancreatectomy (ODP) [8, 11]. The rates of clinically relevant pancreatic fistula formation after LDPS for PDAC were reported to range from 0 to 17 % [14, 18–21]. In most cases of LDPS, resection of the pancreatic parenchyma was performed using a stapler, because it is much simpler and easier to resect and close the pancreatic parenchyma using a stapler than performing intracorporeal suturing techniques for LDPS. Ferrone et al. [28] reported that using a stapler does not significantly reduce the fistula rates after DP. It is thus necessary to invent innovative devices to prevent the development of pancreatic fistulas after LDPS. Laparoscopic approaches using a magnified view have a potential advantage in that there is improved visualization of the anatomy for the resection of complex vessels or lymphadenectomy along appropriate planes during LDPS for PDAC. Several reports, including a meta-analysis, demonstrated that the patients who underwent a LDP had significantly lower estimated blood loss compared to those who underwent an ODP [8, 11, 13]. Even in the cases of PDAC, Magge et al. [18] reported that the mean intraoperative blood loss was significantly lower in the LDPS group compared to the ODPS group (290 vs. 570 mL, p = 0.006). Several reports described that perioperative blood transfusion in PDAC has been linked to decreased patient survival [29, 30]. Therefore, from the viewpoint of the outcome, it may be important to avoid using a blood transfusion in order to improve the long-term prognosis. However, other reports about LDPS for PDAC stated that there were no significant differences in the intraoperative blood loss between the LDPS group and ODPS group [15, 19–21]. The basic concept of the curative surgical resection for PDAC is complete en bloc resection of the tumor, with the resection of regional lymph nodes. The number of dissected lymph nodes and the R0 resection rate are thus the most important factors affecting the long-term oncological outcomes of PDAC. Several research groups have found that the number of dissected lymph nodes in LDPS is similar to that in ODPS. Kooby et al. [15] reported that there was no significant difference in the number of dissected lymph nodes between their LDPS (14.0  ±  8.6) and ODPS (12.3   ±  8.3) groups. They also observed that there were no significant differences in the R0 resection rates between the LDPS (74 %) and ODPS (66 %) groups. Rehman et al. [20] recently demonstrated that the median number of dissected lymph nodes was 16 for LDPS versus 14 for ODPS (p  = 0.53), and the R0 resection rate was 88 % in LDPS cases compared with 86 % in ODPS cases (p  = 0.794). Although reports comparing LDPS and ODPS for PDAC have been rare, the above-cited reports support the use of the laparoscopic approach for the resection of PDAC in the

100

5.2

Overall 5-year survival: 20.0 %

body and tail of the pancreas as an oncologically feasible and safe surgical procedure. The length of hospital stay can provide a valid measure of the invasiveness of a surgical procedure. Hu et al. [21] reported that their LDPS group had significantly shorter hospital stays compared to their ODPS group (5.2  ±  2.5 vs. 8.6   ±  3.9, p  = 0.01) for PDAC. Rehman et al. [20] reported that the total hospital stay was significantly shorter in their LDPS group, with a median of 8 (range, 5–14) days versus 12 (6–21) days in the ODPS group (p  = 0.05). In most of the reports that compared LDPS and ODPS for PDAC, there was a significant between-group difference in the length of hospital stay. However, these findings concerning the length of hospital stay were likely affected by a bias, because the studies were retrospective and the sample sizes were small. The length of hospital stay affects the healthcare cost. Abu Hilal et al. [31] reported that the average perioperative, postoperative and overall costs were £6039, £4547 and £10587 for an LDP group versus £5231, £10094 and £15324 for the ODP group of patients with pancreatic diseases, including PDAC, with values of p  = 0.033, p = 0.006 and p = 0.197, respectively. In their study, the median hospital stay was 7 days (range 3–25 days) in the LDP group versus 11 days (range 5–46 days) in the ODP group (p  = 0.007). These results revealed another advantage of the laparoscopic approach, in terms of the reduced length of the postoperative hospital stay, without a negative impact on cost. On the other hand, Fox et al. [32] reported that the total hospital cost for an ODP was higher than that for an LDP ($13,656.87 vs. $10,842.23, p = 0.03).

0 0

14.8

Overall 5-year survival: 55.6 % Overall 3-year survival: 82 % 12.3 8 100 88 0 12.5 25 37

10.5 16

17 39

11

86

6

Median survival: 16 months Overall 2-year survival: 85.2 % Median survival: 19 months, overall 3-year survival: 30 % No differences in propensity-adjusted overall survival compared to open DP 7.4 9.5 NA 74 92 90 NA NA NA NA NA NA

14 10.3 7.4

Median survival: 14 months 8 77 14.5 0 NA

  Including robot-assisted (n = 4)

NA not available

  Including robot-assisted (n = 8)

b

150

100 11 Hu et al. [21]

0

0 0 445.8 306 Rehman et al. [20]

324.3 376 12 8 Lee et al. [19]b

0 317 28 Magge et al. [18]a

290

422 NA NA 238.4 225 NA

0 0 NA

720 310

Fernandez-Cruz 13 et al. [14] Kooby et al. [15] 23 Song et al. [16] 24 Marangos et al. [17] 21

0

Long‑term oncological outcomes

a

No. of retrieved lymph nodes Pancreatic fistula B–C (%) Morbidity (%) Mortality (%) Blood loss (mL) Length of operation (min) No. of PDACs Authors

Table 1  The main published series of laparoscopic distal pancreatectomy (LDP) for pancreatic ductal adenocarcinoma (PDAC)

R0 resection (%)

Hospital stay (days)

Long-term oncological outcomes

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Randomized controlled trials or large-scale studies are needed to evaluate and clarify the benefits of LDPS with regard to the long-term oncological outcome. However, to the best of our knowledge, there has been no randomized or large-scale study comparing the oncological outcomes of PDAC after LDPS and those after ODPS. Based on a matched comparison analysis in a multicenter retrospective study, Kooby et al. [15] reported that there were no significant differences in the overall survival for PDAC between LDPS (n  = 23, median survival 16 months) and ODPS (n  = 70, median survival 16 months) (p  = 0.71). Magge et al. [18] reported that they found no significant differences in the propensity-adjusted overall survival between LDPS and ODPS for PDAC (hazard ratio, 1.11; p  = 0.80). Rehman et al. [20] reported that the overall three-year survival rates were similar (LDPS = 82 %, ODPS = 74 %; p = 0.89). Hu et al. [21] reported that the 1-, 3- and 5-year survival rates were 100.0 versus 96.0 %,

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57.0 versus 44.0 % and 22.0 versus 20.0 % (ODPS versus LDPS, all p > 0.05), respectively. However, Lee et al. [19] reported that minimally invasive surgery, including LDPS, resulted in longer disease-free survival and overall survival compared to ODPS (disease-free survival: 47.6 vs. 24.7 months, p = 0.027; overall survival: 60.0 vs. 30.7 months, p = 0.046). Port-site metastasis is one of the most serious and unresolved problems of laparoscopic surgery for intra-abdominal malignancies. Although the exact etiology of port-site metastasis is unclear, various factors related to laparoscopic surgery have been suggested, including pneumoperitoneum with carbon dioxide, high intra-abdominal pressure, aerosolization, depression of the local immune function and direct wound contamination [33, 34]. Reports of cases of port-site metastasis of PDAC following laparoscopic pancreatic surgery are rare [35], and thus, the true frequency of port-site metastasis of PDAC is difficult to document. The prevention of port-site metastasis of PDAC requires that the surgeons performing LDPS have adequate training and experience for the proper handling of the tumor.

Conclusions Laparoscopic distal pancreatosplenectomy (LDPS) is a technically feasible and safe surgical procedure for not only benign and low-malignant tumors, but also for PDAC. In addition, LDPS can be oncologically feasible compared to conventional laparotomy in light of its favorable rate of R0 resection and lymph node harvest. LDPS using a magnified view for the laparoscopic approach has the advantage of providing improved visualization of the anatomy for the resection of complex vessels or lymphadenectomy along appropriate planes for PDAC compared to ODPS. However, at the present time, we recommend that LDPS for PDAC be performed by highly skilled laparoscopic pancreatic surgeons with an experienced surgical team at highvolume pancreatic surgery centers. Large randomized and controlled prospective studies are needed to confirm the superiority of LDPS over conventional ODPS.

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Laparoscopic distal pancreatosplenectomy for pancreatic ductal adenocarcinoma.

Laparoscopic distal pancreatectomy (LDP) including laparoscopic distal pancreatosplenectomy has rapidly developed as a minimally invasive surgery. LDP...
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