Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours: a multicentre, open-label, randomised controlled trial

doi:10.1016/S2468-1253(21)00054-6

The Lancet Gastroenterology & Hepatology

Volume 6, Issue 6, June 2021, Pages 438-447

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https://doi.org/10.1016/S2468-1253(21)00054-6 Get rights and content

Summary

Background

The benefit and safety of laparoscopic pancreatoduodenectomy (LPD) for the treatment of pancreatic or periampullary tumours remain controversial. Studies have shown that the learning curve plays an important role in LPD, yet there are no randomised studies on LPD after the surgeons have surmounted the learning curve. The aim of this trial was to compare the outcomes of open pancreatoduodenectomy (OPD) with those of LPD, when performed by experienced surgeons.

Methods

In this multicentre, open-label, randomised controlled trial done in 14 Chinese medical centres, we recruited patients aged 18–75 years with a benign, premalignant, or malignant indication for pancreatoduodenectomy. Eligible patients were randomly assigned (1:1) to undergo either LPD or OPD. Randomisation was centralised via a computer-generated system that used a block size of four. The patients and surgeons were unmasked to study group, whereas the data collectors, outcome assessors, and data analysts were masked. LPD and OPD were performed by experienced surgeons who had already done at least 104 LPD operations. The primary outcome was the postoperative length of stay. The criteria for discharge were based on functional recovery, and analyses were done on a modified intention-to-treat basis (ie, including patients who had a pancreatoduodenectomy regardless of whether the operation was the one they were assigned to). This trial is registered with Clinicaltrials.gov, number NCT03138213.

Findings

Between May 18, 2018, and Dec 19, 2019, we assessed 762 patients for eligibility, of whom 656 were randomly assigned to either the LPD group (n=328) or the OPD group (n=328). 31 patients in each group were excluded and 80 patients crossed over (33 from LPD to OPD, 47 from OPD to LPD). In the modified intention-to-treat analysis (297 patients in the LPD group and 297 patients in the OPD group), the postoperative length of stay was significantly shorter for patients in the LPD group than for patients in the OPD group (median 15·0 days [95% CI 14·0–16·0] vs 16·0 days [15·0–17·0]; p=0·02). 90-day mortality was similar in both groups (five [2%] of 297 patients in the LPD group vs six [2%] of 297 in the OPD group, risk ratio [RR] 0·83 [95% CI 0·26–2·70]; p=0·76). The incidence rate of serious postoperative morbidities (Clavien-Dindo grade of at least 3) was not significantly different in the two groups (85 [29%] of 297 patients in the LPD group vs 69 [23%] of 297 patients in OPD group, RR 1·23 [95% CI 0·94–1·62]; p=0·13). The comprehensive complication index score was not significantly different between the two groups (median score 8·7 [IQR 0·0–26·2] vs 0·0 [0·0–20·9]; p=0·06).

Interpretation

In highly experienced hands, LPD is a safe and feasible procedure. It was associated with a shorter length of stay and similar short-term morbidity and mortality rates to OPD. Nonetheless, the clinical benefit of LPD compared with OPD was marginal despite extensive procedural expertise. Future research should focus on identifying the populations that will benefit from LPD.

Funding

National Natural Science Foundation of China and Tongji Hospital, Huazhong University of Science and Technology, China.

Introduction

Pancreatoduodenectomy is one of the most challenging abdominal operations and remains the standard treatment for pancreatic and periampullary tumours.¹ Traditionally, the procedure was done using the open technique (open pancreatoduodenectomy or OPD). Since the first description of laparoscopic pancreatoduodenectomy (LPD) by Gagner in 1994, the number of specialised centres doing LPD has increased considerably.² However, LPD has a long learning curve, and its benefits and safety over OPD are not clear.2, 3, 4, 5, 6

Research in context

Evidence before this study

Studies have shown that the learning curve plays an important role in laparoscopic pancreatoduodenectomy (LPD), yet there are no studies on LPD versus open pancreatoduodenectomy (OPD) after the surgeons have surmounted the learning curve. We did a systematic literature search for randomised controlled trials that compared LPD with OPD and were published in English up to Dec 31, 2019. The results yielded two single-centre trials (PLOT and PADULAP) and one multicentre trial (LEOPARD-2). Both single-centre trials showed the superiority of LPD over OPD regarding the length of hospital stay. However, the multicentre trial concluded that there was no difference between groups in time to functional recovery, and LPD was associated with more complication-related deaths than OPD.

Added value of this study

To our knowledge, this is the largest multicentre, open-label, randomised controlled trial of LPD versus OPD that has been completed, done by experienced surgeons who have surmounted the learning curve. Participating surgeons were strictly selected from high-volume centres and had done at least 104 LPD operations, which satisfied the requirements of passing the learning curve. Postoperative length of stay was shorter in the LPD group than in the OPD group. 90-day mortality and the rate of serious postoperative morbidities (Clavien-Dindo grade of ≥3) were similar in both groups.

Implications of all the available evidence

The results of this trial suggest that, in highly experienced hands, LPD is a safe and feasible procedure with outcomes similar to OPD. However, even for sufficiently trained pancreatic surgeons, LPD resulted in only a small reduction in length of stay. The indications for and benefits of LPD deserve further research.

Despite three randomised controlled trials (RCTs) on LPD published between 2017 and 2019, there are still insufficient data to recommend LPD over OPD.7, 8, 9 Two single-centre RCTs (PLOT and PADULAP), and most other studies, found that LPD was associated with a shorter hospitalisation time than OPD, but they found no difference in mortality and morbidity between the two procedures.8, 9, 10, 11, 12, 13 However, one multicentre RCT (LEOPARD-2) was prematurely stopped because of safety concerns, as 90-day mortality was higher in the LPD group than in the OPD group.⁷ The results of the three RCTs that compared LPD with OPD have been disputed because of their small sample sizes and the potential negative effects of the long LPD learning curve.14, 15, 16 A broad consensus exists that LPD should be limited to experienced surgeons at high-volume centres, and that trials should be done only in centres where the LPD learning curve has been completed.17, 18 However, the number of LPD operations required to surmount the learning curve is still controversial. Our previous study estimated that 104 operations were needed, which was significantly more than in other studies.¹⁹ Hence, large multicentre RCTs, consisting of experienced surgeons who have surmounted the learning curve, are required to understand the potential benefits and drawbacks of LPD compared with OPD.

To further evaluate the safety and efficacy of LPD relative to OPD, the Minimally Invasive Treatment Group in the Pancreatic Disease Branch of China's International Exchange and Promotion Association for Medicine and Healthcare (MITG-P-CPAM) launched a multicentre RCT in May, 2018. In this Article, we present the short-term outcomes of LPD and OPD from this trial.

Section snippets

Study design and participants

A multicentre, parallel-group, open-label, RCT comparing LPD with OPD was done at 14 medical centres of the MITG-P-CPAM group in China. These participating centres performed at least 50 pancreatoduodenectomies annually, of which at least 20 were laparoscopic. The trial protocol has been published previously and is shown in the appendix (pp 4–25).²⁰ The research protocol was approved by the Ethics Committee of Tongji Hospital and by each participating centre's institutional review board. All

Results

Between May 18, 2018, and Dec 19, 2019, 656 patients, of the 762 we initially assessed, were randomly assigned to the LPD group (n=328) or the OPD group (n=328). We excluded 62 patients before they received surgery (31 in the LPD group and 31 in the OPD group) because of patient withdrawal, preoperatively detected distant metastasis, total pancreatectomy, gastrojejunostomy and biliojejunostomy, cardiopulmonary function insufficiency, allergy, and cerebrovascular accident (figure 1). A total of

Discussion

To our knowledge, this was the largest multicentre RCT done to date showing that LPD was associated with a shorter postoperative length of stay than OPD. The reduced length of stay was statistically significant, but the benefit was clinically marginal despite procedural expertise. Moreover, mortality, postoperative complications, and pathological and oncological outcomes did not differ significantly between the LPD and OPD groups. It is worth mentioning that both operations were done by highly

Data sharing

All of the individual participant data collected during this trial after de-identification will be shared with investigators for whom the proposed use of the data has been approved by an independent review committee and the hospital clinical research department of Tongji Hospital, Wuhan, China. Proposals or written requests for access should be directed to [email protected]. Data requestors will need to sign a data access agreement.

Declaration of interests

All authors declare no competing interests.

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Cited by (139)

Effect of robotic versus open pancreaticoduodenectomy on postoperative length of hospital stay and complications for pancreatic head or periampullary tumours: a multicentre, open-label randomised controlled trial
2024, The Lancet Gastroenterology and Hepatology
The flexibility of the robotic system in resection and reconstruction provides potential benefits in pancreaticoduodenectomy. Increasingly, robotic pancreaticoduodenectomy (RPD) has been reported with favourable outcomes, but high-level evidence is still scarce. We aimed to compare the short-term postoperative outcomes of RPD with those of open pancreaticoduodenectomy (OPD), and hypothesised that postoperative length of hospital stay would be shorter after RPD than after OPD.
This multicentre, open-label randomised controlled trial was conducted at three high-volume hospitals in China. Patients were considered for participation in this trial if they were aged 18–75 years, had a resectable benign, premalignant, or malignant tumour in the pancreatic head or periampullary region; and were suitable for both RPD and OPD. Patients with distant metastases were excluded. Block randomisation was done with random block sizes of four, stratified by centre. Allocation was concealed via individual, sequentially numbered, opaque sealed envelopes. Eligible patients were randomly assigned to the RPD group or the OPD group in a 1:1 ratio by a masked research assistant. Surgeons and patients were not masked to trial group, but data collectors, postoperative outcome assessors, and data analysts were. All patients underwent RPD or OPD according to previously reported techniques. Participating surgeons had surpassed the learning curves of at least 40 RPD and 60 OPD procedures. The primary outcome was postoperative length of hospital stay, which was analysed in the modified intention-to-treat (mITT) population. This trial is registered with the Chinese Clinical Trial Registry (ChiCTR2200056809) and is complete.
Between March 5 and Dec 20, 2022, 292 patients were screened for eligibility, of whom 164 were enrolled and randomly assigned to the RPD group (n=82) or the OPD group (n=82). 161 patients who underwent surgical resection were included in the mITT analysis (81 in the RPD group and 80 in the OPD group). 94 (58%) participants were male and 67 (42%) were female. Postoperative length of hospital stay was significantly shorter in the RPD group than in the OPD group (median 11·0 days [IQR 9·0 to 19·5] vs 13·5 days [11·5 to 18·0]; median difference –2·0 [95% CI –4·0 to 0·0]; p=0·029). During a follow-up period of 90 days, six (7%) of 81 patients in the RPD group and five (6%) of 80 patients in the OPD group required readmission. Reasons for readmission were intra-abdominal haemorrhage (one in each group), vomiting (two in the RPD group and one in the OPD group), electrolyte disturbance (one in each group), and fever (two in each group). There were two (1%) in-hospital deaths within 90 days of surgery, one in each group. The postoperative 90-day mortality rate (difference –0·02% [–5·6 to 5·5]; p=1·00) and the incidence of severe complications (ie, Clavien-Dindo grade ≥3; difference –1·5% [–14·5 to 11·4]; p=0·82) were similar between the two groups.
For surgeons who had passed the learning curve, RPD was safe and feasible with the advantage of shorter postoperative length of hospital stay than OPD. Future research should focus on the medium-term and long-term outcomes between RPD and OPD.
None.
Robotic versus open partial pancreatoduodenectomy (EUROPA): a randomised controlled stage 2b trial
2024, The Lancet Regional Health - Europe
Open partial pancreatoduodenectomy (OPD) represents the current gold standard of surgical treatment of a wide range of diseases of the pancreatic head but is associated with morbidity in around 40% of cases. Robotic partial pancreatoduodenectomy (RPD) is being used increasingly, yet, no randomised controlled trials (RCTs) of RPD versus OPD have been published, leaving a low level of evidence to support this practice.
This investigator-initiated, exploratory RCT with two parallel study arms was conducted at a high-volume pancreatic centre in line with IDEAL recommendations (stage 2b). Patients scheduled for elective partial pancreatoduodenectomy (PD) for any indication were randomised (1:1) to RPD or OPD with a centralised web-based tool. The primary endpoint was postoperative cumulative morbidity within 90 days, assessed via the Comprehensive Complication Index (CCI). Biometricians were blinded to the intervention, but patients and surgeons were not. The trial was registered prospectively (DRKS00020407).
Between June 3, 2020 and February 14, 2022, 81 patients were randomly assigned to RPD (n = 41) or OPD (n = 40), of whom 62 patients (RPD: n = 29, OPD: n = 33) were analysed in the modified intention to treat analysis. Four patients in the OPD group were randomised, but did not undergo surgery in our department and one patient was excluded in the RPD group due to other reason. Nine patients in the RPD group and 3 patients in the OPD were excluded from the primary analysis because they did not undergo PD, but rather underwent other types of surgery. The CCI after 90 days was comparable between groups (RPD: 34.02 ± 23.48 versus OPD: 36.45 ± 27.65, difference in means [95% CI]: −2.42 [−15.55; 10.71], p = 0.713). The RPD group had a higher incidence of grade B/C pancreas-specific complications compared to the OPD group (17 (58.6%) versus 11 (33.3%); difference in rates [95% CI]: 25.3% [1.2%; 49.4%], p = 0.046). The only complication that occurred significantly more often in the RPD than in the OPD group was clinically relevant delayed gastric emptying. Procedure-related and overall hospital costs were significantly higher and duration of surgery was longer in the RPD group. Blood loss did not differ significantly between groups. The intraoperative conversion rate of RPD was 23%. Overall 90-day mortality was 4.8% without significant differences between RPD and OPD.
In the setting of a very high-volume centre, both RPD and OPD can be considered safe techniques. Further confirmatory multicentre RCTs are warranted to uncover potential advantages of RPD in terms of perioperative and long-term outcomes.
Federal Ministry of Education and Research (BMBF: 01KG2010).
Minimally invasive pancreaticoduodenectomy: A favorable approach for frail patients with pancreatic cancer
2024, Surgery (United States)
Within the past decade, minimally invasive pancreaticoduodenectomy has been increasingly adopted in high-volume cancer centers. Amid broader trends of a growing older population, the numbers of frail patients with cancer are expected to increase. In this study, we compared the postoperative outcomes of open pancreaticoduodenectomy and minimally invasive pancreaticoduodenectomy in frail patients with pancreatic ductal adenocarcinoma.
Using the pancreatectomy-targeted American College of Surgeons–National Surgical Quality Improvement Program database (2014–2021), we identified pancreaticoduodenectomy cases for pancreatic ductal adenocarcinoma. Patients with a modified frailty index ≥2 were considered frail. We performed 2:1 (open pancreaticoduodenectomy to minimally invasive pancreaticoduodenectomy) optimal pair propensity score matching for both patient- and disease-specific characteristics. We evaluated baseline covariate balance for homogeneity and assessed 30-day postoperative outcomes: complications, discharge destination, major morbidity, and mortality.
We identified 3,143 frail patients who underwent pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. Of those, 275 (9%) underwent minimally invasive pancreaticoduodenectomy. Minimally invasive pancreaticoduodenectomy was associated with a lower rate of any complications compared with open pancreaticoduodenectomy (43% vs 54%; P < .001), major morbidity (29% vs 35%; P = .042), and nonhome discharge (12% vs 17%; P = .022). When comparing the 2 minimally invasive pancreaticoduodenectomy approaches, robotic surgery was associated with fewer complications compared with laparoscopy (39% vs 51%; P = .040) and a lower mortality rate (1% vs 4%; P = .041)
In frail patients with pancreatic cancer, minimally invasive pancreaticoduodenectomy was associated with better postoperative outcomes than open pancreaticoduodenectomy. This study builds on growing literature reporting that, when properly implemented, minimally invasive pancreaticoduodenectomy is associated with more favorable postoperative outcomes. Given the particularly high risk of complication in frail patients, implementing a preoperative frailty assessment can provide valuable insights to inform patient counseling.
Trends in access to minimally invasive pancreaticoduodenectomy for pancreatic cancers
2024, HPB
Minimally invasive pancreaticoduodenectomy (MIPD), including robotic (RPD) and laparoscopy (LPD), is becoming more frequently employed in the management of pancreatic ductal adenocarcinoma (PDAC), though the majority of operations are still performed via open approach (OPD). Access to technologic advances often neglect the underserved. Whether disparities in access to MIPD exist, remain unclear.
The National Cancer Database (NCDB) was queried (2010–2020) for patients who underwent pancreatoduodenectomy for PDAC. Cochran–Armitage tests assessed for trends over time. Social determinants of health (SDH) were compared between approaches. Multinomial logistic models identified predictors of MIPD.
Of 16,468 patients, 80.03 % underwent OPD and 19.97 % underwent MIPD (22.60 % robotic; 77.40 % laparoscopic). Black race negatively predicted LPD (vs white (OR 0.822; 95 % CI 0.701–0.964)). Predictors of RPD included Medicare/other government insurance (vs uninsured or Medicaid (OR 1.660; 95 % CI 1.123–2.454)) and private insurance (vs uninsured or Medicaid (OR 1.597; 95 % CI 1.090–2.340)). Early (2010–2014) vs late (2015–2020) diagnosis, stratified by race, demonstrated an increase in Non-White patients undergoing OPD (13.15 % vs 14.63 %; p = 0.016), but not LPD (11.41 % vs 13.57 %;p = 0.125) or RPD (14.15 % vs 15.23 %; p = 0.774).
SDH predict surgical approach more than clinical stage, facility type, or comorbidity status. Disparities in race and insurance coverage are different between surgical approaches.
Robot-assisted versus laparoscopic pancreatoduodenectomy: a pan-European multicenter propensity-matched study
2024, Surgery (United States)
The use of robot-assisted and laparoscopic pancreatoduodenectomy is increasing, yet large adjusted analyses that can be generalized internationally are lacking. This study aimed to compare outcomes after robot-assisted pancreatoduodenectomy and laparoscopic pancreatoduodenectomy in a pan-European cohort.
An international multicenter retrospective study including patients after robot-assisted pancreatoduodenectomy and laparoscopic pancreatoduodenectomy from 50 centers in 12 European countries (2009–2020). Propensity score matching was performed in a 1:1 ratio. The primary outcome was major morbidity (Clavien–Dindo ≥III).
Among 2,082 patients undergoing minimally invasive pancreatoduodenectomy, 1,006 underwent robot-assisted pancreatoduodenectomy and 1,076 laparoscopic pancreatoduodenectomy. After matching 812 versus 812 patients, the rates of major morbidity (31.9% vs 29.6%; P = .347) and 30-day/in-hospital mortality (4.3% vs 4.6%; P = .904) did not differ significantly between robot-assisted pancreatoduodenectomy and laparoscopic pancreatoduodenectomy, respectively. Robot-assisted pancreatoduodenectomy was associated with a lower conversion rate (6.7% vs 18.0%; P < .001) and higher lymph node retrieval (16 vs 14; P = .003). Laparoscopic pancreatoduodenectomy was associated with shorter operation time (446 minutes versus 400 minutes; P < .001), and lower rates of postoperative pancreatic fistula grade B/C (19.0% vs 11.7%; P < .001), delayed gastric emptying grade B/C (21.4% vs 7.4%; P < .001), and a higher R0-resection rate (73.2% vs 84.4%; P < .001).
This European multicenter study found no differences in overall major morbidity and 30-day/in-hospital mortality after robot-assisted pancreatoduodenectomy compared with laparoscopic pancreatoduodenectomy. Further, laparoscopic pancreatoduodenectomy was associated with a lower rate of postoperative pancreatic fistula, delayed gastric emptying, wound infection, shorter length of stay, and a higher R0 resection rate than robot-assisted pancreatoduodenectomy. In contrast, robot-assisted pancreatoduodenectomy was associated with a lower conversion rate and a higher number of retrieved lymph nodes as compared with laparoscopic pancreatoduodenectomy.
International survey on opinions and use of robot-assisted and laparoscopic minimally invasive pancreatic surgery: 5-year follow up
2024, HPB
Evidence on the value of minimally invasive pancreatic surgery (MIPS) has been increasing but it is unclear how this has influenced the view of pancreatic surgeons on MIPS.
An anonymous survey was sent to members of eight international Hepato-Pancreato-Biliary Associations. Outcomes were compared with the 2016 international survey.
Overall, 315 surgeons from 47 countries participated. The median volume of pancreatic resections per center was 70 (IQR 40–120). Most surgeons considered minimally invasive distal pancreatectomy (MIDP) superior to open (ODP) (94.6%) and open pancreatoduodenectomy (OPD) superior to minimally invasive (MIPD) (67.9%). Since 2016, there has been an increase in the number of surgeons performing both MIDP (79%–85.7%, p = 0.024) and MIPD (29%–45.7%, p < 0.001), and an increase in the use of the robot-assisted approach for both MIDP (16%–45.6%, p < 0.001) and MIPD (23%–47.9%, p < 0.001). The use of laparoscopy remained stable for MIDP (91% vs. 88.1%, p = 0.245) and decreased for MIPD (51%–36.8%, p = 0.024).
This survey showed considerable changes of MIPS since 2016 with most surgeons considering MIDP superior to ODP and an increased use of robot-assisted MIPS. Surgeons prefer OPD and therefore the value of MIPD remains to be determined in randomized trials.

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ArticlesLaparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours: a multicentre, open-label, randomised controlled trial

Summary

Background

Methods

Findings

Interpretation

Funding

Introduction

Section snippets

Study design and participants

Results

Discussion

Data sharing

Declaration of interests

J Am Coll Surg

Lancet Gastroenterol Hepatol

J Am Coll Surg

Lancet Gastroenterol Hepatol

Hepatobiliary Pancreat Dis Int

Surgery

Surgery

Surgery

Midwifery

Lancet Gastroenterol Hepatol

J Gastrointest Surg

Population-level symptom assessment following pancreaticoduodenectomy for adenocarcinoma

JAMA Surg

Laparoscopic pancreaticoduodenectomy for periampullary tumors: lessons learned from 500 consecutive patients in a single center

Surg Endosc

Comparing short-term and oncologic outcomes of minimally invasive versus open pancreaticoduodenectomy across low and high volume centers

Ann Surg

Minimally invasive versus open pancreaticoduodenectomy for cancer: practice patterns and short-term outcomes among 7061 patients

Ann Surg

Outcomes of a multicenter training program in laparoscopic pancreatoduodenectomy (LAELAPS-2)

Ann Surg

Comparison of perioperative outcomes between laparoscopic and open approach for pancreatoduodenectomy: the PADULAP randomized controlled trial

Ann Surg

Randomized clinical trial of laparoscopic versus open pancreatoduodenectomy for periampullary tumours

Br J Surg

Articles
Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours: a multicentre, open-label, randomised controlled trial