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Review  |  Open Access  |  26 Sep 2024

Minimally invasive left pancreatectomy for pancreatic ductal adenocarcinoma: review of the current literature

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Mini-invasive Surg 2024;8:20.
10.20517/2574-1225.2023.123 |  © The Author(s) 2024.
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Abstract

The minimally invasive approach has gained popularity in the last decades, even in complex abdominal surgery such as pancreatic resections. Currently, many meta-analyses focus on the benefits and advantages of the minimally invasive approach compared to open surgery, especially during left pancreatectomy (LP). Limited data on the oncological outcomes are available. The review aims to describe the surgical and oncological outcomes of the minimally invasive left pancreatectomy (MILP). The search terms were based on the final histological pathology (pancreatic adenocarcinoma) and the comparison of different surgical approaches (open vs. minimally invasive). The search strategy was constructed in PubMed and adapted to run across other database platforms, focusing on studies published until 2022. A total of 2,878 studies were selected and duplicates were removed. After title and abstract screening, 109 articles remained for full-text assessment, of which 28 met the eligibility criteria for this systematic review. Considering the study design, the studies were divided into retrospective (n = 15), prospective (n = 4), and 13 propensity score-matched (n = 9). The present review of the literature suggests that MILP is technically feasible and safe for treating body and tail pancreatic ductal adenocarcinoma (PDAC). MILP did not have any impact on the major complications, reducing hospitalization. Regarding the oncological outcomes, the surgical technique did not have an impact on the R0 resection rate, lymph node harvested rate, use of adjuvant chemotherapy, and overall survival. Further prospective randomized trials remain indicated to assess the oncological impact of the MILP in patients with PDAC.

Keywords

Pancreatic cancer, laparoscopic distal pancreatectomy, robotic distal pancreatectomy, pancreatic resection

INTRODUCTION

The minimally invasive approach to the left-side pancreatic lesions is, actually, considered safe, feasible, and quite easy in expert hands. However, no consensus and robust data in the literature are obtained regarding the use of the minimally invasive approach in the treatment of pancreatic cancer [pancreatic ductal adenocarcinoma (PDAC)]. Since the first report by Gagner in 1996[1], the laparoscopic approach to left pancreatectomy (LP) has gained popularity worldwide, becoming the gold-standard approach for benign and low-grade malignancy lesions of the pancreatic body-tail. The introduction of robotic platforms for performing LP in 2002 contributed to the widespread adoption of minimally invasive pancreatic surgery (MIPS)[2].

After an initial phase where the studies primarily focused on evaluating the safety and feasibility of MIPS on benign or pre-neoplastic lesions, the main effort of the scientific community forthwith changed to try to assess the adequacy and safety of the oncological treatment of PDAC[3]. Although the 2019 Miami guidelines encouraged adopting the minimally invasive approach for all left-side pancreatic lesions, skepticism persisted within the surgical community[4]. This skepticism was highlighted in two recent international surveys, where 19% to 31% of surgeons believed minimally invasive left pancreatectomy (MILP) to be inferior to open LP (OLP) in patients with PDAC[5,6].

Several studies comparing the MILP to OLP consider short-term or surgical outcomes. Few studies focused on the oncological results. However, most of them reported data about all the malignant pancreatic lesions without focusing on PDAC. A large Cochrane review tried to analyze the MILP series on PDAC. The report included 12 studies, demonstrating that different surgical techniques did not have any impact on oncological outcomes, such as tumor negative resection margins (R0), recurrence, and survival. However, all included studies were of very low quality[7].

Recently, data of the literature improved in quality due to the publication of large multicenter or propensity-matched cohort studies. This systematic review aims to compare the short-term and oncological outcomes of patients who underwent minimally invasive vs. open left pancreatic resections.

METHODS

This systematic review was conducted following the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines [Figure 1] and the Cochrane Handbook for Systematic Reviews of Interventions[8,9].

Minimally invasive left pancreatectomy for pancreatic ductal adenocarcinoma: review of the current literature

Figure 1. The PRISMA study selection flowchart. PRISMA: Preferred reporting items for systematic reviews and meta-analyses.

Literature search

The search terms were derived from the final histological pathology (PDAC) and a comparison of different surgical approaches (open vs. minimally invasive). The search strategy was designed in PubMed and adapted for Ovid and Web of Science databases, focusing on studies published until 2022. The PubMed research was as follows:

((((((“Pancreatic Neoplasms”[Mesh]) OR pancreatic adenocarcinom* [tiab]) OR malignan* [tiab]) OR tumo* [tiab])) AND (((((“Pancreatectomy”[Mesh]) OR distal pancreatectom* [tiab]) OR left pancreatectom* [tiab]) OR spleno pancreatectom* [tiab]) OR pancreatosplenectom* [tiab])) AND ((((“Laparoscopy”[Mesh]) OR laparoscop* [tiab]) OR robot* [tiab]) OR minimally invasive* [tiab]).

Eligibility criteria

Studies must report a comparison of different surgical approaches, such as minimally invasive surgery (laparoscopic or robotic) versus open surgery for the treatment of PDAC in the distal pancreas. Non-English studies, duplicates, editorials, animal studies, and studies involving children were excluded. If the outcomes of interest were not reported or indirectly inferable, the study was also excluded. Small case series (< 10 cases per surgical approach) were not selected for the review. Studies reporting data extracted from national or international databases were screened and only the most recent study was included.

Study selection

Two reviewers (MDP and AC) independently screened the research results based on titles and abstracts, followed by full-text evaluation for eligibility. The full-text eligibility selection was conducted independently by MDP and AC following the Scottish intercollegiate guidelines network (SIGN) methodology[10,11]. Any conflicts were resolved using discussion until a consensus was reached.

Risk of bias

Two independent reviewers (MDP and AC) assessed the study quality according to the Newcastle Ottawa Scale (NOS) for all studies since no randomized controlled trials (RCTs) were expected to be included. The NOS checklist consisted of three different quality parameters: comparability of groups, selected population, and assessment of either the exposure or outcome of interest for case-control or cohort studies. A final score was assigned to each study, ranging from 0 to 9. Studies with a score of 7 or higher were considered high-quality.

Inclusion criteria

The studies included must be written in English, report a study population of more than 20 patients who underwent LP for PDAC, and describe intra-, postoperative, and oncological parameters. To avoid data overlap, the most informative or recent article was considered if the data provided came from the same Institution’s database.

Exclusion criteria

Abstracts, case series, no comparing analysis, review articles, partial or incomplete data reporting, case reports, animal studies, studies involving children, or non-English manuscripts were excluded from the systematic review.

Data extraction

Two different reviewers (MDP and AC) extracted data following a predefined evidence table. Data consisted of study design, study period, country, sample size, type of surgical approach, demographic information [age, body mass index (BMI), American Society of Anesthesiology (ASA) score, neoadjuvant therapy], intraoperative characteristics (operative time, estimated blood loss, vascular resection, multi-visceral resection, and conversion rate), postoperative outcomes (postoperative major complications classified by Clavien-Dindo[12], postoperative pancreatic fistula, post pancreatectomy hemorrhage, delayed gastric empty, and length of hospital stay), and oncological outcomes (R0 resection, harvested lymph nodes, adjuvant chemotherapy, and survival). All pancreas-specific complications were classified by the International Study Group of Pancreatic Surgery (ISGPS) definitions[13-15].

RESULTS

Search results

The literature research resulted in 2,878 studies identified, removing the duplicates. After screening titles and abstracts, 109 articles remained for full-text assessment, of which 28 met the eligibility criteria for this systematic review[3,16-42]. Based on the study design, the papers were categorized as retrospective (n = 14), prospective (n = 4), and propensity score-matched (n = 10) studies. Figure 1 illustrates the PRISMA study selection flowchart.

Methodological quality

As shown in Table 1, most included studies were of moderate to high quality (NOS ≥ 6). Only four studies were designed as prospective analyses. Ten studies used propensity score-matched analysis to compare the surgical approaches. Half of the studies were conducted in the Western Countries. Laparoscopy was the most common minimally invasive approach used. Seven articles reported both, laparoscopic and robotic, surgical procedures, while only a recent Chinese paper compared robotic and OLPs.

Table 1

Methodological quality of the manuscripts

AuthorStudy periodCountryStudy designN of patientsDetails of MISQuality
MILPOLP
Retrospective studies
Anderson2010-2012USARetrospective5051,302LLP (51)/RLP (454)8
Chopra2008-2019USARetrospective10541LLP (17)/RLP (88)6
Hao2013-2017ChinaRetrospective4146LLP6
Huang2014-2018ChinaRetrospective2031LLP5
Hu2007-2011ChinaRetrospective1123LLP8
Hirashita2007-2019JapanRetrospective1931LLP5
Kantor2010-2013USARetrospective3491,205LLP6
Kooby2000-2008USARetrospective2370LLP7
Magge2002-2010USARetrospective2834LLP (20)/RLP (8)8
Sharpe2010-2011USARetrospective144625LLP7
Sulpice2007-2012FranceRetrospective3472,406LLP8
Zhang2003-2013ChinaRetrospective1734LLP7
Zhang2012-2018ChinaRetrospective2523LLP6
Zhang2010-2014ChinaRetrospective2276LLP6
Prospective studies
Bauman2005-2014USAProspective3346LLP (28)/RLP (5)7
Plotkin2011-2014USAProspective166335LLP (130)/RLP (36)7
Shin2006-2013KoreaProspective7080LLP8
Stauffer1995-2014USAProspective4428LLP7
Propensity score matching studies
Balduzzi2007-2015ItalyPropensity score matching4444LLP8
Chen2004-2020ChinaPropensity score matching8686LLP6
Chen2010-2019ChinaPropensity score matching6666LLP7
Kwon2010-2017KoreaPropensity score matching156156\7
Lee2007-2010KoreaPropensity score matching1040LLP (8)/RLP (4)8
Lee2009-2017KoreaPropensity score matching35105LLP7
Raoof2010-2013USAPropensity score matching563563LLP8
Van Hilst2007-2015DutchPropensity score matching340340LLP (324)/RLP (16)8
Watson 2010-2016USAPropensity score matching805805\8
Weng2011-2019ChinaPropensity score matching170166RLP8

Minimally invasive left pancreatectomy vs. open left pancreatectomy

A total of 28 studies on MILP vs. OLP were included in the systematic review. Overall, 4,254 and 8,807 patients were submitted to MILP and OLP, respectively. The growth of the minimally invasive approach is evidenced by the increased use of robotic platforms, with 660 robotic procedures reported in studies published after 2010, compared to 125 robotic distal pancreatectomies before 2010.

Few data were reported about the baseline and demographic characteristics of the patients [Supplementary Table 1]. Most studies reported no significant differences between the groups in terms of age, BMI, and ASA score. The open approach was preferred for surgical exploration post-chemotherapy, as reported in a large series by Sharpe et al. and Plotkin et al. Conversion rate had a high variation across the studies ranging from 0% to 40%[25,31] [Supplementary Table 2]. Table 2 and Supplementary Table 2 summarize the intraoperative outcomes. Since the first study, the minimally invasive approach reported an improvement in the operating time and estimated blood loss. A recent propensity score-matching study from Weng et al. reported a significant reduction in the median operative time (120 vs. 180 min, P < 0.001) comparing the robotic approach to the OLP[43]. The better results were more evident in analyzing the estimated blood loss. Almost all the studies reported a decrease in blood loss during the MIDP across the study period. Indeed, considering two large propensity score-matching studies by Van Hilst et al. and Chen et al., both reported significant improvements in the intraoperative bleeding control (200 vs. 300 mL, P < 0.001; 195 vs. 210 mL, P < 0.01, respectively)[35,40]. Major vessel resections were poorly described and, most of the time, involved venous resection and an open approach.

Table 2

Intraoperative and postoperative outcomes

AuthorProcedureOperation timeP valueBlood lossP valueCD > 2 complicationsP valuePostoperative
hospital stay
P value
Retrospective studies
AndersonMIS 505
Open 1,302
N.A.\N.A.\N.A.\6 (5-8)
7 (6-10)
< 0.001
ChopraMIS 105
Open 41
280 (174-416)
248 (181-334)
0.001181 (50-606)
200 (100-450)
0.11923%
10%
0.4146 (5-8)
7 (5.5-7)
0.695
HaoLAP 41
Open 46
411.0 ± 106.2
355.8 ± 72.7
NS294.4 ± 247.5
338.6 ± 230.0
0.4103%
2%
0.5007.9 ± 1.4
11.5 ± 2.7
< 0.001
HuangLAP 20
Open 31
273.8 ± 90.3
264.3 ± 77.1
0.692252.5 ± 198.3
472.6 ± 428.0
0.0375%
3%
0.26319.0 ± 9.9
19.6 ± 16.8
0.876
HuLAP 11
Open23
150.0 ± 54.0
160.0 ± 48.0
0.445100 (50-400)
150 (50-350)
0.678N.A.\5.2 ± 2.5
8.6 ± 3.9
0.010
HirashitaLAP 19
Open 31
397.0 ± 78.0
319.0 ± 80.0
0.001299.0 ± 237.0
576.0 ± 78.0
0.034N.A.\21.5 ± 10.5
29.4 ± 23.3
0.171
KantorMIS 349
Open 1,205
N.A.\N.A.\N.A.\7.1 ± 6.0
8.7 ± 7.3
< 0.001
KoobyLAP 23
Open 189
238.4 ± 68.1
230.4 ± 80.4
0.065422.0 ± 473.0
790.0 ± 828.0
0.040N.A.\7.4 ± 3.4
10.7 ± 6.3
0.030
MaggeMIS 28
Open 34
317.0 ± 23.0
294.0 ± 24.0
NS290.0 ± 60.0
570.0 ± 80.0
0.0060%
9%
0.7306 (IQR: 3)
8 (IQR: 2.75)
0.030
SharpeLAP 144
Open 625
N.A.\N.A.\N.A.\6.8 ± 4.6
8.9 ± 7.5
< 0.001
SulpiceLAP 347
Open 2,406
N.A.\N.A.\7%
10%
0.02814.9 ± 8.9
19.6 ± 14.6
< 0.001
ZhangLAP 25
Open 23
212.2 ± 66.3
203.1 ± 39.7
0.572402.0 ± 258.8
506.5 ± 418.4
0.119N.A.\11.7 ± 5.2
12.9 ± 5.0
0.425
ZhangLAP 22
Open 76
188.0 ± 39.0
160.0 ± 35.0
0.060210.0 ± 130.0
240.0 ± 120.0
0.240N.A.\N.A.\
ZhangLAP 17
Open 34
190 (100-390)
245 (155-420)
0.06450 (30-500)
400 (100-3,900)
< 0.0010%
9%
0.75413 (4-23)
15.5 (6-40)
0.022
Prospective studies
BaumanLAP 33
Open 46
234.0 ± 12.0
252.0 ± 12.0
0.360310.0 ± 68.0
597.0 ± 95.0
0.01615%
22%
0.1007.6 ± 1.4
9.0 ± 0.7
0.440
PlotkinMIS 166
Open 355
239.0 ± 9.0
250.0 ± 6.2
0.311N.A.\10%
15%
0.0245.0 ± 0.31
7.0 ± 0.51
0.009
ShinLAP 70
Open 80
239 (125-397)
254 (115-573)
0.320N.A.\20%
26%
0.3109 (5-29)
12 (7-87)
< 0.001
StaufferLAP 44
Open 28
254 (99-521)
266 (131-543)
0.596322 (10-2650)
874 (150-3,400)
0.00114%
25%
0.3465.1 (2-17)
9.4 (4-36)
< 0.001
Propensity score matching studies
BalduzziLAP 44
Open 44
240 (195-322)
280 (222-379)
0.107290 (70-650)
333 (130-700)
0.49525%
34%
0.3509 (6-13)
13 (8-23)
0.005
ChenLAP 66
Open 66
193.6 ± 49.6
217.5 ± 61.0
0.020195 (80-800)
210 (80-800)
< 0.016%
12%
0.50012 (4-34)
15 (7-42)
< 0.01
ChenLAP 86
Open 86
189.1 ± 45.2
213.3 ± 54.4
< 0.01180 (80-600)
220 (120-800)
< 0.015%
11%
0.3309 (4-34)
13 (7-42)
< 0.01
KwonMIS 156
Open 156
217 ± 56
222 ± 81
0.500N.A.\6%
3%
0.19010.0 ± 5.1
13.4 ± 7.9
< 0.001
LeeMIS 10
Open 40
330.0 ± 168.2
253.3 ± 124.7
0.112440.0 ± 328.0
625.0 ± 879.0
0.366N.A.\12.7 ± 7.1
22.1 ± 27.1
0.050
LeeLAP 35
Open 105
128.0 ± 40.0
170.0 ± 64.0
0.001235.0 ± 240.0
252.0 ± 229.0
0.71811%
15%
0.78211.1 ± 6.7
14.4 ± 7.7
0.026
RaoofLAP 563
Open 563
N.A.\N.A.\N.A.\6 (5-8)
7 (5-9)
< 0.001
Van HilstMIS 340
Open 340
240 (180-295)
230 (178-286)
0.626200 (60-400)
300 (150-500)
< 0.00118%
21%
0.4318 (6-12)
9 (7-14)
< 0.001
WatsonMIS 805
Open 805
N.A.\N.A.\N.A.\6.8 ± 5.5
8.5 ± 7.3
< 0.001
WengRobotic 170
Open 166
120 (110-180)
180 (150-234)
< 0.001100 (50-200)
200 (100-350)
< 0.001N.A.\14 (10-21)
17 (12-24)
0.001

Regarding the postoperative outcomes, the use of the minimally invasive approach did not have any impact on the occurrence of major complications when compared to the OLP. Only large series, such as those by Sulpice et al. and Plotkin et al., reported a favorable outcome in the minimally invasive group (6.6% vs. 10.4%, P = 0.028; 31.0% vs. 42.0%, P = 0.024, respectively)[26,31]. Pancreas-specific complications such as pancreatic fistula, post-pancreatectomy hemorrhage, and delayed gastric emptying were not affected by the surgical approach [Supplementary Table 3].

However, almost the entire cohorts reported in the literature recorded a lower hospital length of stay in the minimally invasive group across all the study designs and periods analyzed. Different minimally invasive approaches, whether laparoscopic or robotic, did not influence the reduction in hospitalization, as demonstrated by large series such as those by Kantor et al. (7.1 ± 6.0 vs. 8.7 ± 7.3 days, P < 0.001), and Weng et al. [14 (10-21) vs. 17 (12-24) days, P = 0.001][22,43].

Table 3 shows the oncological outcomes. The minimally invasive approach was not inferior when compared to OLP regarding the radical resection status. Furthermore, MILP appeared superior to OLP in achieving R0 status. Anderson et al. described a significant increase in the surgical margin disease-free of the minimally invasive resections compared to the open group (85.9% vs. 79.0%, P < 0.001)[16]. Overall, the harvested lymph node rate resulted appropriated, even higher in the minimally invasive group as described by Stauffer et al. (26 vs. 13, P < 0.001)[3]. Two studies by Van Hilst et al. and Weng et al. reported a significant decrease in the number of harvested lymph nodes during MILP (14 vs. 22, P < 0.001; 9 vs. 12, P = 0.003, respectively)[40,43].

Table 3

Oncological outcomes

AuthorProcedureR0 statusP valueHarvested LNP valueAdjuvant chemotherapyP valueOverall survivalP value
Retrospective studies
AndersonMIS 505
Open 1,302
85.9%
79.0%
< 0.00112 (7-19)
12 (7-19)
0.35057.8%
53.8%
0.1103 years 55%
3 years 52%
0.420
ChopraMIS 105
Open 41
69.5%
65.9%
0.53824 (10-56)
20 (9-48)
0.07777.0%
70.7%
0.62833.5 months
28.4 months
0.914
HaoLAP 41
Open 46
88.9%
81.8%
0.7608.7 ± 6
8.4 ± 5.8
0.830N.A.\24.0 months
21.0 months
0.090
HuangLAP 20
Open 31
100.0%
97.0%
0.3159.6 ± 6.4
12.8 ± 5.8
0.20370.0%
80.6%
0.3822 years 50.2%
2 years 38.3%
0.411
HuLAP 11
Open23
100.0%
100.0%
NS14.8 ± 4.5
16.1 ± 5.7
0.875N.A.\42.0 months
54.0 months
NS
HirashitaLAP 19
Open 31
N.A.\14.0 ± 17.0
19.0 ± 18.0
0.84568.0%
68.0%
NSN.A.0.084*
KantorMIS 349
Open 1,205
82.2%
75.1%
< 0.00114.0 ± 11.7
14.8 ± 12.0
0.31067.9%
61.8%
0.05029.9 months
24.0 months
0.090
KoobyLAP 23
Open 189
74.0%
73.0%
0.09813.8 ± 8.4
12.5 ± 8.5
0.47057.0%
70.0%
0.23011.0 months
11.0 months
0.710
MaggeMIS 28
Open 34
86.0%
88.0%
NS11 (8-20)
12 (6-19)
0.750N.A.\N.A.0.800*
SharpeLAP 144
Open 625
87.0%
78.0%
0.04214.9 ± 10.0
13.3 ± 9.9
0.085N.A.\N.A.\
SulpiceLAP 347
Open 2,406
N.A.\N.A.\N.A.\62.5 months
36.7 months
< 0.001
ZhangLAP 25
Open 23
92.0%
95.6%
0.66315.8 ± 6.7
18.2 ± 7.9
0.26892.0%
82.6%
0.71624.5 months
28.7 months
0.633
ZhangLAP 22
Open 76
91.0%
87.0%
0.61011.2 ± 4.6
14.4 ± 5.5
0.440N.A.\29.6 months
27.6 months
0.340
ZhangLAP 17
Open 34
94.1%
85.3%
0.6509 (5-15)
8 (2-22)
0.53476.5%
76.5%
NS14.0 months
14.0 months
0.802
Prospective studies
BaumanLAP 33
Open 46
77.0%
87.0%
0.53014.5 ± 1.1
17.5 ± 1.2
0.07061.0%
63.0%
0.83017.9 months
15.1 months
NS
PlotkinMIS 166
Open 355
N.A.\N.A.\N.A.\N.A.\
ShinLAP 70
Open 80
75.7%
83.8%
0.22012 (1-34)
10 (1-64)
0.13078.6%
68.8%
0.18033.4 months
29.1 months
0.250
StaufferLAP 44
Open 28
95.5%
82.1%
0.10126 (5-48)
13 (1-45)
< 0.00175.6%
75.0%
NS26.6 months
26.4 months
0.851
Propensity score matching studies
BalduzziLAP 44
Open 44
67.0%
48.0%
0.06311 (6-22)
19 (11-30)
0.02371.0%
79.0%
0.75819 months
20 months
0.571
ChenLAP 66
Open 66
97.0%
89.4%
0.00813.4 ± 5.4
11.7 ± 5.1
0.00671.2%
65.2%
0.46019.0 months
17.0 months
0.330
ChenLAP 86
Open 86
96.5%
90.7%
0.12014.4 ± 5.2
12.7 ± 5.0
0.03070.9%
66.3%
0.510N.A.0.500
KwonMIS 156
Open 156
76.3%
64.1%
0.01914.1 ± 8.7
15.6 ± 9.7
0.15066.7%
66.4%
NS34.9 months
24.5 months
0.012
LeeMIS 10
Open 40
100.0%
87.5%
0.42611.7 ± 7.2
12.1 ± 8.1
0.88770.0%
65.0%
0.765N.A.0.053*
LeeLAP 35
Open 105
94.3%
90.5%
0.73012.6 ± 8.1
14.3 ± 10.0
0.380N.A.\N.A.\
RaoofLAP 563
Open 563
85.1%
81.5%
0.11012 (7-18)
11 (6-18.5)
0.759N.A.\3 years 41.6%
3 years 36.0%
0.457
Van HilstMIS 340
Open 340
67.0%
58.0%
0.01914 (8-22)
22 (14-31)
< 0.00176.0%
73.0%
0.56128.0 months
31.0 months
0.774
WatsonMIS 805
Open 805
83.1%
80.0%
0.60513.8 ± 10.3
14.2 ± 10.1
0.52453.4%
51.6%
0.45428.0 months
21.0 months
0.006
WengRobotic 170
Open 166
92.9%
89.2%
0.2249 (4-14)
12 (7-17)
0.00361.8%
67.5%
0.27431.0 months
27.0 months
0.070

The adjuvant treatment rate reported was surprisingly inferior to expectation. The different surgical approaches did not have any impact on this result, even if positive postoperative outcomes have been reported in the minimally invasive group. Comparable results were recorded for the overall postoperative survival. Overall, the surgical approach did not affect the patient’s survival. However, a large series reported some long-term benefits of the MILP. Sulpice et al. analyzed 347 laparoscopic LP, describing a significant improvement in survival in the minimally invasive group (62.5 vs. 36.7 months, P < 0.001)[26]. These data were confirmed by two recent large series by Kwon et al. and Watson et al. that reported a higher overall survival rate of the MILP when compared to OLP (34.9 vs. 24.5 months, P = 0.012; 28.0 vs. 21.0 months, P = 0.006, respectively)[36,41].

DISCUSSION

Despite advances in surgical techniques and the widespread use of minimally invasive approaches for resecting benign and pre-malignant pancreatic tumors, pancreatic resection for adenocarcinoma remains a challenge, even in experienced hands[44].

The results of this systematic review have revealed that MILP was safe and feasible even in the treatment of PDAC. The minimally invasive approach appears to be at least as effective as the open approach in terms of intra- and postoperative outcomes. Furthermore, the minimally invasive technique appeared to reduce both estimated blood loss and hospital length of stay. Regarding oncological outcomes, MILP again proved to be non-inferior when compared to OLP. Particularly, the MILP reached at least the same accuracy as the OLP in the lymphadenectomy and R0 resection.

Since the introduction of MIPS, there has been significant skepticism regarding its short- and long-term outcomes, especially compared to open surgery[45]. Nevertheless, this review clearly demonstrates a growing interest in MIPS over time. Increased use, standardization, and technological advancements have led to improved MIPS outcomes. Indeed, MILP, even when used in treating PDAC, showed advantages over open surgery, including reduced estimated blood loss (11/19 studies), shorter hospital stays (22/27 studies), comparable operative time (14/20 studies), and lower rates of major postoperative complications (15/18 studies).

For left-sided PDAC, the recommended oncological treatment includes resection of the spleen, Gerota’s fascia, and appropriate lymphadenectomy (at least 11 lymph nodes with resection of stations 10, 11, and 18 for pancreatic tail tumors, also adding stations 8 and 9 in case of pancreatic body tumors)[46,47]. In a recent multicenter study involving 1,200 patients from 34 centers, resection of Gerota’s fascia (P = 0.019), R0 resection (P = 0.006), and a decreased lymph node ratio (P < 0.001) were identified as positive prognostic factors for overall survival[46]. Furthermore, two systematic reviews involving PDAC patients who underwent MILP analyzed these oncological outcomes[48,49]. These studies were significantly small, including only 5 and 12 studies with a total of 261 and 1,506 patients, respectively. However, the surgical free resection margin rate and survival reported were similar between the two surgical approaches, though the evidence available was of low quality. In the present study, after reviewing 28 studies, both R0 resection and survival rates were comparable between MILP and OLP (no difference in 19/28 and 22/28 studies, respectively). Additionally, similar results were found when considering the lymph node harvest rate (no difference in 20/28 studies). These findings were supported by the results of the latest RCT on the oncological safety and feasibility of the MILP[50]. The DIPLOMA trial is an international multicenter study that provided the best evidence of the non-inferiority of MILP for radical resection margin rate compared to OLP[50]. Furthermore, the study assessed that the harvested lymph node rate was similar in both groups. MILP was correlated to longer operative times but provided better aesthetic results one year postoperatively. In line with the results of this review, the surgical approach did not affect other postoperative outcomes. However, the authors did not record any benefits for time to functional recovery, estimated blood loss, and length of hospital stay from MILP as has been described in previous RCT performed for all indications[51,52]. To date, three RCTs are ongoing to compare MILP vs. OLP in patients with PDAC: (1) the LAPAN study, promoted by the Japan Clinical Oncology Group study (jRCT 1031220705)[53]; (2) the NCT03792932 trial performed by the Fudan University in China; and (3) the NCT03957135 trial performed by the Seoul National University Hospital in Korea.

Oncological outcomes may be closely linked to surgical outcomes. Indeed, we can assume that a short length of stay and a short time to return to normal activity are associated with a higher adjuvant chemotherapy treatment rate. It is widely recognized that completing adjuvant chemotherapy after PDAC resection is associated with improved overall survival. Recently, a study on 2,440 patients treated with upfront surgery for PDAC, showed that at least 65% of patients did not receive chemotherapy after surgery. Only 7% of the patients completed the adjuvant chemotherapy, while 28% received incomplete treatment[54]. The results of this review underlined the shorter hospitalization of the patients submitted to MILP compared to OLP, recording the same major complication rate. However, no significant difference in adjuvant treatment was reported between the two approaches. This could be explained by the possibility that the MIPS series included smaller tumors in the minimally invasive arm, which may not require adjuvant treatment after neoadjuvant chemotherapy.

The present results should be read carefully due to several limitations and potential selection bias of the included studies. Indeed, the selection criteria for candidates undergoing MIDP varied across studies and are commonly linked to postoperative outcomes. Young patients, with low BMI, small lesions at the first stage, no vascular involvement, and without previous abdominal surgery are more often selected for MILP. The availability of robotic platforms may also contribute to selection bias. Third, the robotic procedures could be performed only in high-volume centers by expert surgeons. Fourth, a clear definition of free surgical margin or R0 resection is unavailable. The heterogeneity of the definitions could affect the oncological data, especially the patient’s survival, as previously reported[55]. Fifth, only one RCT was available. Despite efforts to report more comparable data, using a registry, prospective database, or propensity score matching studies, RCTs remain mandatory to assess the real benefit of MILP in patients affected by PDAC.

CONCLUSIONS

This literature review suggests that MILP is technically feasible and safe for treating pancreatic adenocarcinoma of the body and tail. MILP did not affect major complications but reduced hospitalization time. In terms of oncological outcomes, free surgical resection margin rate, lymph node harvested rate, use of adjuvant chemotherapy, and overall survival were not influenced by the surgical technique. Further prospective randomized trials are warranted to assess the oncological benefit of MILP in patients affected by PDAC.

DECLARATIONS

Authors’ contributions

Conception and design: De Pastena M, Coppola A

Administrative support: De Pastena M, Coppola A

Provision of study materials or patients: De Pastena M, Coppola A

Collection and assembly of data: De Pastena M, Coppola A, Esposito A, Casciani F, Tufo A, Salvia R

Data analysis and interpretation: De Pastena M, Coppola A, Esposito A, Casciani F, Tufo A, Salvia R

Manuscript writing: De Pastena M, Coppola A, Esposito A, Casciani F, Tufo A, Salvia R

Final approval of manuscript: De Pastena M, Coppola A, Esposito A, Casciani F, Tufo A, Salvia R

Availability of data and materials

Not Applicable.

Financial support and sponsorship

None.

Conflicts of interest

All authors declared that there are no conflicts of interest.

Ethical approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Copyright

© The Author(s) 2024.

Supplementary Materials

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Cite This Article

Review
Open Access
Minimally invasive left pancreatectomy for pancreatic ductal adenocarcinoma: review of the current literature
Matteo De PastenaMatteo De Pastena, ... Roberto Salvia

How to Cite

De, Pastena M.; Coppola A.; Esposito A.; Casciani F.; Tufo A.; Salvia R. Minimally invasive left pancreatectomy for pancreatic ductal adenocarcinoma: review of the current literature. Mini-invasive. Surg. 2024, 8, 20. http://dx.doi.org/10.20517/2574-1225.2023.123

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© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, sharing, adaptation, distribution and reproduction in any medium or format, for any purpose, even commercially, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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