Abstract
Introduction
Pancreatic neuroendocrine tumors (PNETs) are rare neoplasms. Minimal access surgery has been the favoured approach for these tumors over the past decade. There is a lack of robust data comparing laparoscopic and robotic pancreatic surgery for PNETs and this has led to the lack of a global conclusion regarding which approach is superior. Thus, we conducted a systematic review and meta-analysis of the available data to compare outcomes following laparoscopic versus robotic pancreatic surgery for pancreatic neuroendocrine tumors.
Methods
Studies reporting outcomes of laparoscopic or robotic surgery for pancreatic neuroendocrine tumors were included. Inverse variance and Mantel-Haenszel statistical analysis methods were used for continuous and dichotomous data, respectively. All outcomes were quantitatively analyzed using the random effects model. The risk of bias was assessed using the ROBINS-1 tool.
Results
A total of 14 studies with 767 patients were included. The mean difference in the operating time was 21.08 min (95% CI: -4.38, 46.54, I2 = 43%), favouring the laparoscopic group. The pooled odds ratio for the rate of formation of the pancreatic fistula was 0.88 (95% CI: 0.54, 1.45, I2 = 0%), favouring the robotic group. Blood loss was higher in the laparoscopic group (MD = -89.72 ml, 95% CI:-143.37 to -36.06, I2 = 93%). Other parameters, including re-exploration rate, length of hospital stay, R0 resection, rate of conversion, and spleen preservation, were similar in both groups.
Conclusion
The robotic approach might be preferable to the laparoscopic approach because of the lower rate of POPF and blood loss. Larger randomised controlled trials are required to ascertain these findings.
Supplementary Information
The online version contains supplementary material available at 10.1007/s00423-025-03662-3.
Keywords: Laparoscopic PNET Surgery, Robotic PNET Surgery, Systematic Review PNET, Metanalysis PNET
Introduction
Pancreatic neuroendocrine tumors (PNETs) are rare neoplasms with a yearly incidence of one per 100,000 individuals [1]. The incidence of functioning pancreatic neuroendocrine tumors is low, and their capacity to produce symptoms is based on the production of various hormones. In the current era, research on pancreatic neuroendocrine tumors has advanced notably, and their treatment has progressed toward a more comprehensive and minimally invasive approach [2].
Surgical resection has been considered a reliable treatment for PNETs as it is associated with improved survival [3]. With the progress in technology, minimally invasive surgery is being increasingly used to ameliorate the surgical trauma and complications associated with open surgery. In 1996, the first laparoscopic distal pancreatectomy was performed by Cuschieri for chronic pancreatitis followed by Gagner, who in the same year, performed laparoscopic surgery for an islet cell tumor [4, 5]. With developments in the robotic surgical system, the first case of robotic distal pancreatectomy (RDP) was reported by Melvin et al. in 2002, marking the dawn of a new era in minimally invasive pancreatic surgery [6]. Robotic surgery with its advantages of a high-definition, three-dimensional vision, along with seven degrees of freedom and better ergonomics has allowed surgeons to overcome certain difficulties associated with laparoscopy.
Pancreatic surgery has conventionally been known to be fraught with high rates of morbidity, predominantly in the form of post-operative pancreatic fistula. It is one of the main determinants that predict a patient’s post-operative course thus making it an important outcome of interest.
Alfieri et al. compared short and long-term outcomes after robot-assisted versus laparoscopic distal pancreatectomy for PNETs and showed that the laparoscopic procedure had a significantly lower spleen preservation rate and higher blood loss [7]. Another comparative study by Zhang et al. showed that patients who underwent robotic surgery had significantly higher spleen preservation rates, reduced blood loss, and better oncological outcomes with a higher lymph node harvest [8].
However, there is a lack of robust data comparing laparoscopic and robotic pancreatic surgery for pancreatic neuroendocrine tumors leading to the lack of a global conclusion. Thus, we conducted a systematic review and meta-analysis of the available data to compare outcomes following laparoscopic versus robotic pancreatic surgery for pancreatic neuroendocrine tumors.
Methods
This systematic review and meta-analysis was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines [9]. The review was registered prospectively in the International Prospective Register of Systematic Reviews (PROSPERO) (CRD42021264562).
Cohort studies and randomized controlled trials reporting outcomes of laparoscopic and robotic pancreatic surgery for pancreatic neuroendocrine tumors were included and case series of the same beyond the year 2000 and with a sample size of more than 10 were included.
Case reports, narrative reviews, expert opinions, studies with no retrievable texts, full English translation, and studies with only abstracts available, were excluded.
Study selection and data extraction
The literature search was done till December 2023 in electronic databases like Medline (PubMed), Ovid (Embase), Scopus, Web of Science, and Cochrane Central Registry of Trials (CENTRAL). The reference lists of all included studies and relevant systematic reviews for additional references were reviewed by two independent observers (DS, OP).
The pair of reviewers (DS, OP) independently screened titles and abstracts and duplicates were removed. The full texts of potentially eligible studies were reviewed to determine the final eligible studies. Disagreements were resolved by discussion with a third reviewer (VKB).
A standardized data extraction form was developed in Microsoft Excel by a reviewer DS. Data extraction was conducted by DS and verified by OP. The form included the first author, publication year, country, population, interventions, and outcomes, such as operating time and postoperative pancreatic fistula, blood loss, re-exploration rate, spleen preservation rate, length of hospital stay, rate of conversion, R0 resection percentage, and mortality. If necessary, DS reached out to study authors for additional information.
Search strategy
The search protocol was based on four search strings: Laparoscopic, Robotic, pancreatic neuroendocrine tumors, and PNETs. The categories were combined in the literature search using the Boolean operator “AND.” Within each category, MeSH terms and text words were combined using the boolean operator “OR.” Search strings for MEDLINE, Embase, Scopus, and Cochrane CENTRAL were used in similar words and strategy.
Final PubMed search strings were: (((“pancreatic neuroendocrine tumors“[All Fields]) OR (PNET)) AND (“laparoscopic“[All Fields]) AND (“robotic“[All Fields])), ((((((“pancreatic neuroendocrine tumors“[All Fields]) OR (PNET)) OR (neuroendocrine tumor)) OR (neuroendocrine tumors)))))) AND ((“laparoscopy“[All Fields]) OR (laparoscopic)) AND (“robotic“[All Fields]) & ((((pancreatic neuroendocrine OR PNET)) OR (laparoscopic)) AND (laparoscopy)) AND (robotic).
Data synthesis and analysis
The primary outcomes were the operating time and postoperative pancreatic fistula (POPF). The definition of POPF is in accordance with the ISGPS definition and grading [10]. The secondary outcomes included blood loss, re-exploration rate, spleen preservation rate, length of hospital stay, rate of conversion, R0 resection percentage, and mortality.
Pooled odds ratio (OR) and 95% confidence intervals (95% CI) were used for dichotomous outcomes such as operative time, blood loss, length of hospital stay, and mean difference (MD), and 95% CI were used for continuous outcomes such as postoperative pancreatic fistula, Re-exploration R0 resection, rate of conversion, spleen preservation, and mortality. For dichotomous data, the Mantel-Haenszel statistical analysis method was used, whereas the inverse variance statistical analysis approach was used for continuous data. Random-effects models to pool study data were used. statistical analyses were carried out using Review Manager version 5.4 [11]. Weighted means were calculated for the non-comparative studies.
Assessment of statistical heterogeneity
The heterogeneity in the meta-analyses was assessed by visual inspection of the Forest plot and by the I2 statistic.
Risk of bias assessment
Using the “Risk of Bias in Non‑randomized Studies of Interventions (ROBINS‑I)” assessment tool [12], two independent researchers DS and MP determined any potential bias in the included non-randomized trials, and any disagreements were settled by discussing with VKB.
Evidence summary
The evidence was summarized both narratively and in GRADE evidence profiles. Four authors (DS, BY, MP, PK) assessed evidence quality using the Grades of Recommendation, Assessment, Development, and Evaluation (GRADE) system. Evidence strength was categorized as high-quality (⊕⊕⊕⊕), moderate-quality (⊕⊕⊕⊖), low-quality (⊕⊕⊖⊖), or very low-quality (⊕⊖⊖⊖). Consensus resolved any discrepancies.
Funding
There was no funding for this study.
Results
The total number of titles obtained using the search terms in all the databases mentioned was 9758. They were screened independently by two reviewers (DS, OP) and duplicates were removed. The total number of titles after removal of duplicates was 9728 out of which 142 abstracts were selected for review. Of the selected abstracts, 23 full-text articles were assessed for their eligibility. The final number of studies included in the analysis was 14 (Fig. 1) [7, 8, 13–24].
Fig. 1.
PRISMA flowchart
There were three non-randomized comparative studies, eight retrospective cohort studies, and three retrospective case series. A total of 767 patients were included in this study. The sample size of the three comparative studies was 276 (35.9%). The weighted mean age of the laparoscopic group was 44.5 years (range, 20–95 years) and the robotic group was 28.4 years (range, 25–77 years). The mean tumor size was 23.4 mm (range, 2–130 mm) in the laparoscopic group and 16.3 mm (range, 3–40 mm) in the robotic group.
Risk of bias assessment
The risk of bias assessment for individual studies is shown in Fig. 2. All studies showed a low risk of bias in all aspects except for the bias due to missing data, and confounding which was unclear. The overall certainty of evidence for all the outcomes is shown in the supplementary table.
Fig. 2.
“Risk of Bias in Non‑randomized Studies—of Interventions. (ROBINS‑I)” assessment tool
Primary outcomes
Operating time
Three studies with 276 patients in both groups showed no significant difference in operating time between the two groups (MD = 21.08 min, 95% CI: -4.38, 46.54, low level of evidence), with moderate heterogeneity between the studies (I2 = 43%) [7, 8, 22]. The weighted mean of 11 studies was 253.88 min (range, 133–417.4 min) in the laparoscopic group and 188.20 min (range, 117–270 min) in the robotic group [13–21, 23, 24]. (Fig. 3(a), Tables 1, 2, 3 and 4)
Fig. 3.
Forest plot showing analysis of (a): Operating time. (b): Incidence of Postoperative pancreatic fistula. (c): Intraoperative blood loss
Table 1.
Preoperative parameters
| Year | Author | n= | Surgery performed | N | Male | Female | Age (Years) |
SD/ Range | |
|---|---|---|---|---|---|---|---|---|---|
| 2016 | Nell S [22] | 21 | Lap | 14 | 7 | 7 | 35 | 8.8 | |
| Robotic | 7 | 4 | 3 | 30 | 11 | ||||
| 2017 | Zhang J [8] | 74 | Lap | 31 | 12 | 19 | 48.7 | 12.3 | |
| Robotic | 43 | 20 | 23 | 47.9 | 10.5 | ||||
| 2019 | Alfieri S [25] | 181 | Lap | 85 | 43 | 42 | |||
| Robotic | 96 | 46 | 50 | ||||||
| 2015 | Xourafas D [23] | 73 | Lap | 73 | 41 | 32 | 61 | 20–95 | |
| 2019 | Di Benedetto [13] | 12 | Rob | 12 | 6 | 6 | 53.8 | 25–77 | |
| 2016 | Tian F [14] | 60 | Rob | 60 | 21 | 39 | 45.2 | 13.2 | |
| 2016 | Shi Y [15] | 26 | Rob | 26 | 11 | 15 | 50.1 | 14.1 | |
| 2017 | Cienfuegos F [16] | 36 | Lap | 36 | 17 | 23 | 55.1 | 12.1 | |
| 2019 | Kim H [17] | 58 | Lap | 58 | 18 | 40 | 49.5 | 12 | |
| 2008 | Fernández-Cruz [18] | 49 | Lap | 49 | 6 | 43 | 58.8 | 22–83 | |
| 2018 | Han SH [24] | 42 | Lap | 42 | 21 | 21 | 53 | 30–75 | |
| 2013 | Haugvik SP [19] | 65 | Lap | 65 | 31 | 34 | 59 | 21–87 | |
| 2011 | Hu M [20] | 43 | Lap | 43 | 19 | 24 | 42.4 | 14.5 | |
| 2011 | Zhao YP [21] | 27 | Lap | 27 | 9 | 18 | 44.7 | 18.6 | |
Table 2.
Primary outcomes
| Author | Group | Tumor size (mm) | SD/Range | Operating time (min) | SD/Range | POPF | A | B | C |
|---|---|---|---|---|---|---|---|---|---|
| Nell S | Lap | 17 | 5–17 | 268 | 9 | 4 | 4 | 1 | |
| Robotic | 25 | 19–40 | 185 | 4 | 1 | 3 | 0 | ||
| Zhang J | Lap | 16 | 12–22 | 133.4 | 41.8 | 12 | 7 | 4 | 1 |
| Robotic | 16 | 13–25 | 139.3 | 56.9 | 11 | 7 | 4 | 0 | |
| Alfieri S | Lap | 233.7 | 65.6 | 34 | 17 | 15 | 2 | ||
| Robotic | 270.2 | 90.2 | 40 | 20 | 17 | 3 | |||
| Xourafas D | Lap | 22 | 2-130 | 352 | 16 | 12 | 4 | 0 | |
| Di Benedetto | Robotic | 11 | 3–15 | 203.17 | 3 | 2 | 1 | 0 | |
| Tian F | Robotic | 13.7 | 3.4 | 117 | 6 | 0 | 6 | 0 | |
| Shi Y | Robotic | 23 | 12 | 124.6 | 50.9 | 12 | 5 | 7 | 0 |
| Cienfuegos F | Lap | 20.5 | 13 | 287.8 | 99.1 | 13 | |||
| Kim H | Lap | 26 | 13 | 417.4 | 102.7 | 24 | 21 | 3 | 0 |
| Fernández-Cruz | Lap | 47 | 25–110 | 10 | 6 | 3 | 1 | ||
| Han SH | Lap | 13 | 6–52 | 168.5 | 29 | 25 | 4 | ||
| Haugvik SP | Lap | 22 | 5–95 | 175 | 14 | 1 | 13 | 0 | |
| Hu M | Lap | 210.5 | 56.6 | 9 | 2 | 4 | 3 | ||
| Zhao YP | Lap | 15 | 5 | 178.5 | 68.3 | 11 |
Table 3.
Secondary outcomes
| Author | Group | Blood loss (ml) | Re-exploration | Spleen preservation | LOHS (days) |
Conversion | R0 resection |
|---|---|---|---|---|---|---|---|
| Nell S | Lap | 100 (0-3500) | 0 | 7 (3–41) | 6 | 6 | |
| Robotic | 50 (50–400) | 0 | 7 | 7 (5–12) | 0 | 6 | |
| Zhang J | Lap | 200 | 1 | 1 | 14.4 (7.2) | 0 | 31 |
| Robotic | 50 | 0 | 0 | 12.8 (6.8) | 0 | 43 | |
| Alfieri S | Lap | 239.7 (112) | 4 | 38 | 10 (7.4) | 12 | 84 |
| Robotic | 162.5 (98) | 6 | 64 | 11 (8.8) | 9 | 96 | |
| Xourafas D | Lap | 6 | 5 (3–18) | 11 | 71 | ||
| Di Benedetto | Robotic | 38.3 (20–110) | 0 | 3.9 | 0 | ||
| Tian F | Robotic | 32.5 (10-1000) | 0 | 12 (6–36) | 3 | 60 | |
| Shi Y | Robotic | 76 (85.4) | 0 | 22.6 (15.6) | 0 | ||
| Cienfuegos F | Lap | 3 | 21 | 6 (0.9) | 0 | 36 | |
| Kim H | Lap | 433.2 (394) | 1 | 12.6 (6.1) | 55 | ||
| Fernández-Cruz | Lap | 1 | 37 | 6.3 (5–14) | 49 | ||
| Han SH | Lap | 175 | 0 | 7 (4–18) | 40 | ||
| Haugvik SP | Lap | 300 (5-2700) | 5 | 7 (2–27) | 4 | 39 | |
| Hu M | Lap | 132.5 (155.7) | 2 | 9.1 (5.6) | |||
| Zhao YP | Lap | 124.8 (133.9) | 0 | 15.1 (7.8) | 19 |
Table 4.
Weighted mean of parameters
| Group | Age (years) |
Tumor size (mm) | Operative time (min) | POPF (total) (Grade) |
Blood loss (ml) | Re-exploration | Spleen preservation | LOHS (days) |
Conversion | R0 Resection | Mortality | ||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| A | B | C | |||||||||||
| Lap | 44.51 | 23.4 | 253.88 | 34.6% | 190.4 | 4.39% | 48.25% | 10.49 | 15.7% | 90.7% | 1.7% | ||
| 60.5% | 34.3% | 5% | |||||||||||
| Robotic | 28.4 | 16.31 | 188.20 | 31.1% | 92.15 | 2.45% | 50.6% | 12.33 | 4.9% | 99.5% | 0.4% | ||
| 46% | 50% | 3.9% | |||||||||||
Post-operative pancreatic fistula
Among the comparative studies, the POPF rate for robotic group was 55/140 (39.2%) as compared to 55/130 (42.3%) in laparoscopic group. The forest plot favoured the robotic group with an odds ratio of 0.88 and a heterogeneity of 0% (OR = 0.88, 95% CI: 0.54, 1.45, low level of evidence). On comparison of weighted percentages of 14 studies, the rate of POPF was almost equal in both groups (34.6% and 31.1% respectively for the laparoscopic and robotic groups). The percentages of grades A, B, and C in the laparoscopic group were 60.5%, 34.3%, and 5%, and the robotic group was 46%, 50%, and 3.9% respectively. (Fig. 3b), Table 4)
Secondary outcomes
Blood loss
Three studies with 276 patients in both groups showed a significantly lower incidence of blood loss in the robotic group than in the laparoscopic group (MD = -89.72 ml, 95% CI:-143.37 to -36.06, moderate level of evidence), with considerable heterogeneity between the studies (I2 = 93%). Overall, 12 studies reported data on blood loss. The weighted mean was 190.4 ml and 92.1 ml in the laparoscopic and robotic groups respectively. (Fig. 3(c), Table 4)
Re-exploration
There was no significant difference in re-exploration rates between the two groups among the three studies (OR = 1.06, 95% CI: 0.32, 3.53, low level of evidence), with no heterogeneity between studies (I2 = 0%). All the 14 studies reported data on re-exploration. The weighted percentage of re-exploration was 4.39% and 2.45% in the laparoscopic and robotic groups. (Fig. 4(a), Table 4)
Fig. 4.
Forest plot showing analysis of (a): Re-exploration rates. (b): Length of hospital stay. (c): R0 resection
Length of hospital stay
Three studies with 276 patients in both groups showed no significant difference in the length of hospital stay between the two groups (MD = 0.10 days, 95% CI: -1.80 to 1.99, low level of evidence) with no heterogeneity between the studies (I2 = 0%). The weighted mean length of hospital stay from 14 studies was 10.4 days in the laparoscopic group and 12.3 days in the robotic group. (Fig. 4(b), Table 4)
R0 resection
There was no significant difference in R0 resection rates between the two groups among the three studies (OR = 5.94, 95% CI: 0.88, 39.93, low level of evidence), with no heterogeneity between studies (I2 = 0%). Overall, ten studies reported data on R0 resection. The weighted percentage of R0 resection was 90.7% and 99.5% in the laparoscopic and robotic groups respectively. (Fig. 4(c), Table 4)
Rate of conversion
There was no significant difference in the conversion rate between the two groups among the three studies (OR = 0.40, 95% CI: 0.08–2.09, low level of evidence), with moderate heterogeneity between studies (I2 = 35%). The weighted percentage of the rate of conversion from 10 studies reporting the data was 15.7% and 4.9% in the laparoscopic and robotic groups respectively. (Fig. 5(a), Table 4)
Fig. 5.
Forest plot showing analysis of (a): Rate of conversion.(b): Spleen preservation rates
Spleen preservation
There was no significant difference in spleen preservation rates between the two groups in the two studies (OR = 1.32, 95% CI: 0.17–10.24, very low level of evidence), with moderate heterogeneity between studies (I2 = 50%). The weighted percentage of spleen preservation in four studies was 48.25% and 50.6% in the laparoscopic and robotic groups, respectively. (Fig. 5(b), Table 4)
Mortality
There was no mortality in either of the comparative studies. Eight studies reported data on mortality, and the weighted percentage from these studies were 1.7% and 0.4% in the laparoscopic and robotic groups, respectively. (Table 4)
Discussion
Several minimally invasive techniques for the management of PNETs have been developed in an attempt to reduce morbidity and improve the outcomes of pancreatic surgery. Owing to the location of the pancreas, laparoscopy has several limitations owing to restricted mobility and two-dimensional visualization. With the introduction of robotics in surgery, recent literature has shown good results with robotic surgery for pancreatic neuroendocrine tumors.
The primary outcomes of this study were the operative time and incidence of POPF following laparoscopic versus robotic resection of PNETs. These results suggest that the rate of POPF was similar among the three comparative studies. However, the incidence of POPF was lower in the robotic group. The rate and grade of pancreatic fistula were higher in the laparoscopic group in a study by Nell et al. The number of patients operated on by the laparoscopic approach was double that of those operated on by the robotic technique, which might have led to this result. Similarly, in a study by Zhang et al., the rate and grade of fistula formation were higher in the laparoscopic group. In a study by Alfieri et al., the rate of POPF was slightly higher (41.7% vs. 40%) in the robotic group. Considering the details of the three comparative studies, there is no evidence to suggest the superiority of the robotic over the laparoscopic approach.
The slightly higher incidence of POPF in the laparoscopic group obtained in this meta-analysis arose mainly from the difference in the POPF rates in the study by Nell et al. Other factors include the technique of closure of the pancreatic stump, which needs to be accounted for when comparing the rate of POPF in laparoscopic and robotic approaches. Patients operated upon by the robotic technique are likely to undergo stump closure by stapler along with sutures, which might be a plausible explanation for the results.
These are all small case series or comparative studies, and there is limited literature comparing laparoscopic and robotic surgery for pancreatic neuroendocrine tumors.
The other primary outcome of this study was the operating time. Three comparative studies were analyzed, of which two favored the laparoscopic group. However, these results were not statistically significant [7, 8]. An important consideration when comparing the operating times is the inclusion or exclusion of the docking time. The study by Alfieri et al. separately reported the docking time, which was not mentioned in the study by Zhang et al. The inclusion of docking time in the operating time might be responsible for the longer operating time in the robotic group. In contrast, a third comparative study by Nell et al. reported a shorter operating time in the robotic group. However, in their study, the percentage of enucleations (36% vs. 29%) was higher in the laparoscopic group, which may explain the results.
With regards to the extent of resection, the robotic approach seemed to achieve a higher rate of R0 resection. A total of 145/146 and 121/130 patients underwent R0 resection in the robotic and laparoscopic groups, respectively. The p value was approaching significance with an odds ratio of 5.94. Therefore, it can be inferred that the robotic approach might lead to a higher R0 resection rate. The majority of the long-term data compared laparoscopic and open approaches, and most of those studies were non-randomized with a selection bias towards the inclusion of smaller tumors in the laparoscopic group. It might be extrapolated that a better R0 resection rate might ultimately lead to higher overall survival. Long-term randomized studies are required to shed light on this hypothesis.
Blood loss was significantly lower in the robotic group, with a mean difference of 89 ml. The mean weighted blood loss was also lower in the robotic group (92 mL vs. 190 ml). Better 3D visualization, dexterity, and choice of smaller tumors for the robotic approach might be plausible reasons. All patients who underwent robotic surgery in the non-comparative studies underwent enucleation rather than resection, which could explain the lower blood loss in the robotic group. Among the comparative studies, two reported that patients underwent distal pancreatectomy. The third study by Nell et al. did not report on the type of procedure. The study by Kim et al. reported a mean blood loss of approximately 400 ml in 58 patients which skewed the weighted average blood loss towards a higher side in the laparoscopic group.
The rate of spleen preservation was reported in two comparative studies and was found to be higher in the robotic group, with an odds ratio of 1.32. The weighted percentage also favoured the robotic group, although the difference was small (50.6% vs. 48.25%, respectively). There are several small vessels connecting the pancreatic body and tail, and the splenic artery and vein. The vascular walls are easily ruptured during dissection, making safe separation of the pancreatic body and tail from splenic vessels a key point of spleen preserving surgery. Robot-assisted systems can effectively improve the dissection of splenic vessels and creation of the retro-pancreatic tunnel, thus improving the safety of surgery and rate of spleen preservation. None of the non-comparative studies commented upon rates of spleen preservation in the robotic group. Furthermore, only two non-comparative studies reported the rate of spleen preservation (68.2%) in the laparoscopic group.
The robotic approach favoured the rate of conversion with an odds ratio of 0.4 in the two comparative studies. The weighted percentage conversion was also higher in the laparoscopic group. The study by Alfieri et al. reports that the authors were adequately experienced in the robotic approach which resulted in low conversion rates in their study. Other comparative studies have not commented on the experience of surgeons in using laparoscopic and robotic approaches.
The rates of re-exploration were similar in the comparative studies, with an odds ratio of 1.04. The large comparative study by Alfieri et al. reported a lower re-exploration rate in the laparoscopic group (6.7% vs. 4.3%). However, the weighted percentage favoured the robotic group over the laparoscopic group (4.4% vs. 2.5%, respectively). Inclusion of more patients undergoing enucleation rather than resection and a smaller mean tumor size in the robotic arm might be a possible reason for the results.
With regards to mortality, laparoscopic group was found to have a marginally higher mortality (1.7% vs. 0.4%) on comparison of the overall percentage. This might be due to a selection bias towards a better patient profile in the robotic group. However, a lower overall rate of POPF, lower blood loss, higher rate of spleen preservation, higher R0 resection, and lower conversion rate in the robotic group would play a role in achieving lower mortality than the laparoscopic approach.
This is the first metanalysis to selectively compare the role of laparoscopic versus robotic approach for PNETs. Patients treated with newer surgical techniques may be healthier than those undergoing conventional treatments. This selection bias is likely because none of the included studies were randomised and all the studies were retrospective. Nevertheless, it should be noted that PNETs are rare and all patients with PNETs do not satisfy the criteria for surgery, thus making it difficult to carry out prospective randomised studies. The meta-analysis had a component of heterogeneity because of the inclusion of various surgical procedures under one heading, that is laparoscopic or robotic. The experience of the surgeon and cost of treatment, which are important practical considerations, could not be studied. Randomised studies with a larger sample size, although difficult to conduct are needed to strengthen the findings of this study.
In conclusion, robotic approach for pancreatic neuroendocrine tumors might be beneficial over laparoscopic approach in terms of rates of post-operative pancreatic fistula, blood loss, rate of conversion, R0 resection and spleen preservation in appropriately chosen patients. However, large multicentre comparative studies or randomised trials are required to substantiate the results. Long term follow-up comparing laparoscopic and robotic approach is required to comment on the oncological safety of the procedures. The reporting of outcomes of different surgical approaches such as enucleation and excision should be separately reported. The operating time in the robotic group should not include the docking time, which should be separately reported. Finally, surgeon experience, ergonomics and cost are important factors in any treatment approach and should be analysed in future studies.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Author contributions
DS, VS, BY, MP wrote the main manuscript. The concept for the study was given by VKB. DS, OP performed the literature search and disagreements were resolved by VKB. The statistical analysis was done by DS, MP, BY, VS, PK. DS, AK, BY and MP prepared the figures. DS, VS and SR prepared the tables. All authors reviewed the manuscript.
Data availability
No datasets were generated or analysed during the current study.
Declarations
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Ma ZY, Gong YF, Zhuang HK, Zhou ZX, Huang SZ, Zou YP et al (2020) Pancreatic neuroendocrine tumors: A review of serum biomarkers, staging, and management. World J Gastroenterol 26(19):2305 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Chabot J, Editorial (2016) Pancreatic neuroendocrine tumors: primum Non nocere. Surgery 159(1):348–349 [DOI] [PubMed] [Google Scholar]
- 3.Hill JS, McPhee JT, McDade TP, Zhou Z, Sullivan ME, Whalen GF et al (2009) Pancreatic neuroendocrine tumors: the impact of surgical resection on survival. Cancer 115(4):741–751 [DOI] [PubMed] [Google Scholar]
- 4.Cuschieri A, Jakimowicz JJ, van Spreeuwel J (1996) Laparoscopic distal 70% pancreatectomy and splenectomy for chronic pancreatitis. Ann Surg 223(3):280–285 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Gagner M, Pomp A, Herrera MF (1996) Early experience with laparoscopic resections of islet cell tumors. Surgery 120(6):1051–1054 [DOI] [PubMed] [Google Scholar]
- 6.Melvin WS, Needleman BJ, Krause KR, Schneider C, Wolf RK, Michler RE et al (2002) Computer-enhanced robotic telesurgery. Initial experience in foregut surgery. Surg Endosc 16(12):1790–1792 [DOI] [PubMed] [Google Scholar]
- 7.Alfieri S, Butturini G, Boggi U, Pietrabissa A, Morelli L, Vistoli F et al (2019) Short-term and long-term outcomes after robot-assisted versus laparoscopic distal pancreatectomy for pancreatic neuroendocrine tumors (pNETs): a multicenter comparative study. Langenbecks Arch Surg 404(4):459–468 [DOI] [PubMed] [Google Scholar]
- 8.Zhang J, Jin J, Chen S, Gu J, Zhu Y, Qin K et al (2017) Minimally invasive distal pancreatectomy for PNETs: laparoscopic or robotic approach? Oncotarget 8(20):33872–33883 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev 10(1):89 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M et al (2017) The 2016 update of the international study group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 161(3):584–591 [DOI] [PubMed] [Google Scholar]
- 11.RevMan [Internet] [cited 2024 Jul 14]. Available from: https://training.cochrane.org/online-learning/core-software/revman
- 12.ROBINS-I tool | Cochrane Methods [Internet]. [cited 2024 Jul 14]. Available from: https://methods.cochrane.org/robins-i
- 13.Di Benedetto F, Magistri P, Ballarin R, Tarantino G, Bartolini I, Bencini L et al (2019) Ultrasound-Guided robotic enucleation of pancreatic neuroendocrine tumors. Surg Innov 26(1):37–45 [DOI] [PubMed] [Google Scholar]
- 14.Tian F, Hong XF, Wu WM, Han XL, Wang MY, Cong L et al (2016) Propensity score-matched analysis of robotic versus open surgical enucleation for small pancreatic neuroendocrine tumours. Br J Surg 103(10):1358–1364 [DOI] [PubMed] [Google Scholar]
- 15.Shi Y, Peng C, Shen B, Deng X, Jin J, Wu Z et al (2016) Pancreatic enucleation using the Da Vinci robotic surgical system: a report of 26 cases. Int J Med Robot Comput Assist Surg MRCAS 12(4):751–757 [DOI] [PubMed] [Google Scholar]
- 16.Cienfuegos JA, Salguero J, Núñez-Córdoba JM, Ruiz-Canela M, Benito A, Ocaña S et al (2017) Short- and long-term outcomes of laparoscopic organ-sparing resection in pancreatic neuroendocrine tumors: a single-center experience. Surg Endosc 31(10):3847–3857 [DOI] [PubMed] [Google Scholar]
- 17.Kim H, Song KB, Hwang DW, Lee JH, Alshammary S, Kim SC (2019) Laparoscopic versus open pancreaticoduodenectomy for pancreatic neuroendocrine tumors: a single-center experience. Surg Endosc 33(12):4177–4185 [DOI] [PubMed] [Google Scholar]
- 18.Fernández-Cruz L, Blanco L, Cosa R, Rendón H (2008) Is laparoscopic resection adequate in patients with neuroendocrine pancreatic tumors? World J Surg 32(5):904–917 [DOI] [PubMed] [Google Scholar]
- 19.Haugvik SP, Marangos IP, Røsok BI, Pomianowska E, Gladhaug IP, Mathisen O et al (2013) Long-term outcome of laparoscopic surgery for pancreatic neuroendocrine tumors. World J Surg 37(3):582–590 [DOI] [PubMed] [Google Scholar]
- 20.Hu M, Zhao G, Luo Y, Liu R (2011) Laparoscopic versus open treatment for benign pancreatic insulinomas: an analysis of 89 cases. Surg Endosc 25(12):3831–3837 [DOI] [PubMed] [Google Scholar]
- 21.Zhao YP, Zhan HX, Zhang TP, Cong L, Dai MH, Liao Q et al (2011) Surgical management of patients with insulinomas: result of 292 cases in a single institution. J Surg Oncol 103(2):169–174 [DOI] [PubMed] [Google Scholar]
- 22.Nell S, Brunaud L, Ayav A, Bonsing BA, Groot Koerkamp B, van Nieveen EJ et al (2016) Robot-assisted spleen preserving pancreatic surgery in MEN1 patients. J Surg Oncol 114(4):456–461 [DOI] [PubMed] [Google Scholar]
- 23.Xourafas D, Tavakkoli A, Clancy TE, Ashley SW (2015) Distal pancreatic resection for neuroendocrine tumors: is laparoscopic really better than open? J Gastrointest Surg Off J Soc Surg Aliment Tract 19(5):831–840 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Han SH, Han IW, Heo JS, Choi SH, Choi DW, Han S et al (2018) Laparoscopic versus open distal pancreatectomy for nonfunctioning pancreatic neuroendocrine tumors: a large single-center study. Surg Endosc 32(1):443–449 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
No datasets were generated or analysed during the current study.





