Randomized clinical trial

Comparison of the duration of hospital stay after laparoscopic

or open distal pancreatectomy: randomized controlled trial
B. Björnsson1 , A. Lindhoff Larsson1 , C. Hjalmarsson2,3 , T. Gasslander1 and P. Sandström1
1
Department of Surgery and Clinical and Experimental Medicine, Linköping University, Linköping, 2 Department of Surgery, Blekinge Hospital,
Karlskrona, and 3 Department of Clinical Sciences, Lund University, Lund, Sweden
Correspondence to: Dr B. Björnsson, Department of Surgery and Clinical and Experimental Medicine, Linköping University, SE-581-83 Linköping,
Sweden (e-mail: bergthor.bjornsson@liu.se)

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Background: Studies have suggested that laparoscopic distal pancreatectomy (LDP) is advantageous
compared with open distal pancreatectomy (ODP) regarding hospital stay, blood loss and recovery. Only
one randomized study is available, which showed enhanced functional recovery after LDP compared
with ODP.
Methods: Consecutive patients evaluated at a multidisciplinary tumour board and planned for standard
distal pancreatectomy were randomized prospectively to LDP or ODP in an unblinded, parallel-group,
single-centre superiority trial. The primary outcome was postoperative hospital stay.
Results: Of 105 screened patients, 60 were randomized and 58 (24 women, 41 per cent) were included
in the intention-to-treat analysis; there were 29 patients of mean age 68 years in the LDP group and 29
of mean age 63 years in the ODP group. The main indication was cystic pancreatic lesions, followed
by neuroendocrine tumours. The median postoperative hospital stay was 5 (i.q.r. 4–5) days in the
laparoscopic group versus 6 (5–7) days in the open group (P = 0⋅002). Functional recovery was attained
after a median of 4 (i.q.r. 2–6) versus 6 (4–7) days respectively (P = 0⋅007), and duration of surgery was
120 min in both groups (P = 0⋅482). Blood loss was less with laparoscopic surgery: median 50 (i.q.r.
25–150) ml versus 100 (100–300) ml in the open group (P = 0⋅018). No difference was found in the
complication rates (Clavien–Dindo grade III or above: 4 versus 8 patients respectively). The rate of delayed
gastric emptying and clinically relevant postoperative pancreatic fistula did not differ between the groups.
Conclusion: LDP is associated with shorter hospital stay than ODP, with shorter time to functional
recovery and less bleeding. Registration number: ISRCTN26912858 (www.isrctn.com).

Paper accepted 21 January 2020

Published online 7 April 2020 in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.11554

Introduction time to oral intake for laparoscopic compared with

open distal pancreatectomy (ODP)6 . However, only one
Laparoscopic distal pancreatectomy (LDP) was first prospective RCT7 comparing laparoscopic with open dis-
reported over 20 years ago, but widespread implementation tal pancreatectomy has been performed. In the multicentre
has been slow outside a few specialist centres1 . However, LEOPARD trial7 , the laparoscopic group had a shorter
recent nationwide data2 – 4 indicated that laparoscopy time to functional recovery, reduced hospital stay, less
accounted for 40 per cent of distal pancreatectomies perioperative blood loss, and less delayed gastric emptying
at referral centres in the UK between 2006 and 2016, compared with the open group. This came at the expense
and for 60 per cent in Norway between 2012 and 2016, of a longer duration of surgery and a non-significant
although the variation between different regions in the use tendency towards a higher fistula rate in the laparoscopic
of laparoscopy was large. Possible reasons for this include group.
the fact that minimally invasive techniques are not without The need for further comparison of laparoscopic and
challenges, have long learning curves, and risk causing open distal pancreatectomy is evident, and the setting of
harm during the learning process5 . a single centre eliminates differences in local routines and
Pooled data from retrospective cohort studies have traditions, allowing for hospital stay to be the primary end-
shown shorter hospital stays, less blood loss and reduced point. The aim of this study was to compare short-term

© 2020 The Authors. British Journal of Surgery published by John Wiley & Sons Ltd on behalf of BJS Society Ltd. BJS 2020; 107: 1281–1288
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
1282 B. Björnsson A. Lindhoff Larsson, C. Hjalmarsson, T. Gasslander and P. Sandström

Fig. 1 Approach to laparoscopic distal pancreatectomy

a Placement of trocars b Location and removal of the lesion

Portal Coeliac Ligated

vein trunk splenic artery

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Pancreatic
5-mm tumour
trocar position
Splenic Inferior
12-mm vein mesenteric
trocar position vein
Superior Endo
mesenteric stapler
vein

a Four trocars are placed: one above the umbilicus (12 mm); one in the lateral part of the left rectus abdominis muscle (12 mm); one to the left of the xiphoid
process (5 mm); and one in the left flank (5 mm). b The surgeon and assisting surgeon (controlling the camera) stand on the patient’s right side. The left
colonic flexure is mobilized, and the splenocolic ligament divided. The omental bursa is then opened and the stomach mobilized completely, including the
short gastric vessels. The lesion in the pancreas is identified, with or without the help of ultrasonography. The inferior border of the pancreas is dissected. A
band is placed around the pancreas to the right of the lesion (and the splenic vein if splenectomy is intended). Before dividing the pancreas, the splenic artery
is identified and secured using Hem-o-Lok® clips (Teleflex Medical, Research Triangle Park, North Carolina, USA). For spleen-preserving procedures,
the splenic artery is dissected from the pancreas and left intact. To improve visibility of the superior border of the pancreas, the stomach is sutured to
the anterior abdominal wall. Depending on the preoperative assessment, lymphadenectomy is performed as indicated for pancreatic adenocarcinoma. The
pancreas is divided using a linear stapler with a cartridge size based on the thickness of the pancreas. A gradual stepwise compression technique and division
is used, as described previously16 , to reduce the risk of rupture of the pancreas along the staple line. After division of the pancreas, the resection is done in
a medial to lateral direction. The spleen is mobilized (en bloc for splenectomy); the surgical specimen is placed in a plastic bag and retrieved by enlargement
of the trocar incision above the umbilicus.

surgical outcomes following LDP and ODP with the are six referral hospitals in the region, accounting for just
hypothesis that laparoscopy would shorten hospital stay in over half of the population. From these hospitals, patients
patients undergoing standard distal pancreatectomy8 . with hepatopancreatobiliary malignancy are referred to the
trial centre. During the study period, September 2015 to
Methods February 2019, all patients undergoing planned distal pan-
createctomy were screened for participation in the study.
The study protocol was approved by the regional ethics
board in the south-east health region of Sweden on 10
Inclusion and exclusion criteria
June 2015 (dnr. 2015/39-31). The study was registered at
www.isrctn.com on 28 September 2015 (https://doi.org/10 Adult patients with benign or malignant lesions in the body
.1186/ISRCTN26912858). or tail of the pancreas considered resectable with standard
After passing and analysing an institutional learning distal pancreatectomy at a regional tumour board, and not
curve including 37 patients operated on with LDP, a in need of additional simultaneous procedures or extended
randomized 1 : 1, controlled, unblinded, parallel-group, pancreatectomy, were eligible for inclusion in the study.
single-centre superiority trial was designed9 . The study Pregnancy and lactation were exclusion criteria, as was the
protocol has been published previously10 . predefined need to resect organs other than the pancreas
The study was carried out in the south-east health region and spleen, or to divide the pancreas to the right of the
of Sweden, an area with approximately 1⋅1 million inhabi- mesenteric vein. Patients expected to be unable to comply
tants. The study site, Linköping University Hospital, is the with the protocol for reasons of language or cognitive
only hepatopancreatobiliary centre in this region, primarily function, as well as patients younger than 18 years, were
responsible for almost half of the total population. There also excluded.

© 2020 The Authors. British Journal of Surgery published by John Wiley & Sons Ltd www.bjs.co.uk BJS 2020; 107: 1281–1288
on behalf of BJS Society Ltd.
Duration of hospital stay after distal pancreatectomy 1283

Fig. 2 CONSORT diagram for the trial

Assessed for eligibility

n = 105

Excluded n = 45
Enrolment

Did not meet inclusion criteria n = 37

Declined to participate n = 5
Missed inclusion n = 3

Randomized
n = 60

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Allocated to intervention (LDP) n = 30 Allocated to control (ODP) n = 30
Received intervention n = 29 Received ODP n = 28
Allocation

Did not receive intervention n = 1 Did not receive ODP n = 2

Dissemination on preoperative radiology n = 1 Surgery performed at another hospital
(patient excluded) n = 1
Laparotomy and biopsy from peritoneum n = 1
Follow-up

Lost to follow-up n = 0 Lost to follow-up n = 0

Discontinued intervention n = 0 Discontinued ODP n = 0
Analysis

Analysed n = 29 Analysed n = 29
Excluded from analysis n = 0 Excluded from analysis n = 0

LDP, laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.

Randomization surgery, including any readmissions, and functional recov-

ery, defined as the number of postoperative days to reach
Surgeons at the outpatient clinic provided written and
no need for parenteral fluids or drug administration
oral information about the study. Patients who agreed
(except for subcutaneously administered low molecular
to participate signed a written informed consent form.
weight heparin), as well as being ambulatory and able
Randomization was performed with computer-generated
to perform the activities of daily living. Calorie intake
random numbers in blocks of ten (5 : 5). The randomiza-
was not included in the definition of functional recovery,
tion was performed by a research nurse not participating
as absence of parenteral fluid administration was used
in the care of the patients. Sealed, opaque, serially num-
to define adequate intake. Other documented outcomes
bered identical envelopes containing group allocations
were duration of surgery, estimated intraoperative blood
were opened once the patients had agreed to inclusion
loss, 90-day postoperative complications according to
in the trial.
the Clavien–Dindo classification11 , and mortality. Severe
complications were defined as Clavien–Dindo grade III
or above. Complications specifically related to pancreatic
Primary and secondary outcomes
surgery as defined by the International Study Group on
The primary outcome of the study was the length of Pancreatic Surgery, including postoperative pancreatic
postoperative hospital stay, analysed as the initial stay at the fistula (POPF), postoperative delayed gastric emptying
hepatopancreatobiliary centre. (DGE) and postpancreatectomy haemorrhage (PPH) were
Secondary outcomes were: total hospital stay before analysed12 – 14 . The outcomes were cross-checked against
discharge home (including stay at the referral hospital) those registered in the Swedish National Pancreatic and
as well as the total length of stay in the 90 days after Periampullary Cancer Registry15 .

© 2020 The Authors. British Journal of Surgery published by John Wiley & Sons Ltd www.bjs.co.uk BJS 2020; 107: 1281–1288
on behalf of BJS Society Ltd.
1284 B. Björnsson A. Lindhoff Larsson, C. Hjalmarsson, T. Gasslander and P. Sandström

Table 1 Baseline characteristics of patients randomized to Table 2 Primary and secondary outcomes
laparoscopic or open distal pancreatectomy
LDP ODP
LDP ODP (n = 29) (n = 29) P†
(n = 29) (n = 29)
Primary outcome
Age (years)* 68(12) 63(13) Postoperative stay at 5 (4–5) 6 (5–7) 0⋅002
Sex ratio (M : F) 19 : 10 15 : 14 hepatopancreatobiliary
BMI (kg/m2 )* 27(6) 28(6) centre (days)*
ASA grade Secondary outcomes
I 7 5 Discharge to home 14 14 1⋅000
II 9 18 Postoperative stay, including 6 (5–8) 8 (6–10) 0⋅007
referral hospital (days)*
III 13 6

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Readmission 4 6 0⋅487‡
Radiological size of lesion (mm)* 27(11) 31(19)
Total postoperative hospital 6 (5–9) 8 (7–13) 0⋅008
Indication for surgery
stay (90 days) (days)*
IPMN 13 12
Time to functional recovery 4 (2–6) 6 (4–7) 0⋅007
Cystic tumour (excluding IPMN) 3 4 (days)*
Neuroendocrine tumour 4 7
Adenocarcinoma 7 3
*Values are median (i.q.r.). LDP, laparoscopic distal pancreatectomy; OPD,
open distal pancreatectomy. †Mann–Whitney U test, except ‡χ2 test.
Other 2 3
Previous abdominal surgery 16 14
Charlson Co-morbidity Index score† 3 (3–5) 3 (2–4)
Conversion to open surgery
ECOG performance status
0 12 12 Conversion (in the laparoscopic group) was defined as any
1 15 15 incision that was not intended for trocar placement or
2 2 2 removal of the surgical specimen.
From referral hospital 17 15

Values are *mean(s.d.) and †median (i.q.r.). LDP, laparoscopic dis-

tal pancreatectomy; OPD, open distal pancreatectomy; IPMN, intra- Postoperative treatment
ductal papillary mucinous neoplasia; ECOG, Eastern Cooperative
Oncology Group.
All patients were observed in a postoperative recovery
unit for 6 h after surgery, and were then transferred to
the specialized hepatopancreatobiliary unit for the rest of
Laparoscopic distal pancreatectomy (intervention their hospital stay. Ward staff did not participate in any
group) of the operations and were not involved in the study.
A fast-track programme was followed for both patient
A detailed description of the operative procedure has groups. The programme omitted the use of a nasogas-
been published previously10 , and a brief overview given in tric tube directly after surgery (in the operating theatre).
Fig. 1. The pancreas was divided at the portal–mesenteric Oral intake and mobilization were encouraged as soon as
confluence, or to the left of it, with a linear stapler without possible. Epidural anaesthesia was allowed in the ODP
reinforcement (Endo GIA™ Ultra; Medtronic, Min- group (at the anaesthetist’s discretion), but was not used
neapolis, Minnesota, USA). One surgeon performed all routinely in the LDP group. Drains were removed when
laparoscopic pancreatic resections using conventional output was less than 20 ml in 24 h, or when the drain
laparoscopy. The gradual stepwise compression technique amylase level was less than three times the upper serum
and division was applied, as described previously16 . A 24-Fr amylase limit.
passive drain was placed in proximity to the pancreatic
resection line and emerged in the subcostal region on the
left side of the abdominal wall. Statistical analysis
The primary endpoint, length of stay at a hepatopancre-
atobiliary centre, was used for sample size calculations.
Open distal pancreatectomy (control group)
Because LDP has not been associated with an increased
ODP was performed through a midline laparotomy inci- length of stay compared with that for OPD in previous
sion by one of three senior pancreatic surgeons. Division publications, a one-sided sample size calculation was used.
of the pancreas was achieved as described above, and drains Based on previous data9 , mean hospital stay for LDP and
were placed in the same way. ODP were assumed to be 5 and 7⋅5 days respectively. With

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on behalf of BJS Society Ltd.
Duration of hospital stay after distal pancreatectomy 1285

Table 3 Intraoperative and postoperative outcomes

LDP (n = 29) ODP (n = 29) P†

Duration of surgery (min)* 120 (105–140) 120 (103–149) 0⋅482‡

Estimated blood loss (ml)* 50 (25–150) 100 (100–300) 0⋅018‡
Additional resection 2 4 0⋅389
Splenectomy 19 23 0⋅240
Clavien–Dindo complications at 90 days (≥ grade III) 4 8 0⋅195
IIIa 4 5
IIIb 0 1
IVa 0 1

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IVb 0 0
V 0 1
Postoperative pancreatic fistula 9 11 0⋅581
Grade B 9 10
Grade C 0 1
Postoperative delayed gastric emptying 1 5 0⋅085
Grade A 1 2
Grade B 0 1
Grade C 0 2
Postpancreatectomy haemorrhage 1 0 0⋅313
Grade A 1 0
Grade B 0 0
Grade C 0 0

*Values are median (i.q.r.). LDP, laparoscopic distal pancreatectomy; OPD, open distal pancreatectomy. †χ2 or Fisher’s exact test, except ‡ Mann–Whitney
U test.

a standard deviation of 3⋅5, type I error of 0⋅05, and 1 − β Age, sex distribution, size of lesion and other baseline
value of 0⋅8, 25 patients were needed for each group. To characteristics, except for ASA fitness grade, were similar in
account for the risk of drop-outs, a total of 60 patients the two groups (P = 0⋅043). More than half of the patients
were included in the trial. were referred from other hospitals (Table 1).
All statistical analyses were performed in an intention-to- Of 30 patients randomized to LDP, 29 were operated
treat (ITT) manner; all operated patients were analysed on (and included in the analysis); one patient was excluded
according to their group allocation by the randomiza- before any surgery had been performed owing to dissemi-
tion process. Data are presented as the median (i.q.r.) or nated disease found on radiology before the planned opera-
mean(s.d.) values, as appropriate. The primary endpoint, tion. One patient in the laparoscopic group had conversion
hospital stay at the hepatopancreatobiliary centre, was to open surgery due to oozing and slow progression of the
evaluated using the Mann–Whitney U test. Dichoto- dissection (included in the laparoscopy group for ITT anal-
mous variables were assessed with χ2 or Fisher’s exact ysis). Of the 30 patients assigned to ODP, one was excluded
tests, and continuous variables were assessed with the as they were operated on in another hospital; the remain-
independent-samples t test or the Mann–Whitney U ing 29 patients were included in the analysis. One patient in
test, as indicated. A two-sided P < 0⋅050 was considered the open group had a diagnostic laparotomy and biopsy of
statistically significant. All analyses were performed using the peritoneum only (included in the open group for ITT
SPSS® version 26 (IBM Corp., Armonk, New York, USA). analysis), and 28 had an ODP.
The initial hospital stay at the hepatopancreatobiliary
Results centre was 5 (4–5) days in the laparoscopic group com-
pared with 6 (5–7) days in the open group (P = 0⋅002)
During the study period, a total of 105 adults with lesions (Table 2).
in the body or tail of the pancreas were screened for study Estimated intraoperative blood loss was significantly
eligibility. A total 68 patients were found to meet all the reduced in the LDP group compared with that in the ODP
inclusion criteria, of whom 60 patients agreed to participate group, although other intraoperative outcomes were simi-
in the study and were randomized (Fig. 2). lar (Table 3).

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1286 B. Björnsson A. Lindhoff Larsson, C. Hjalmarsson, T. Gasslander and P. Sandström

Table 4 Pathology outcomes

discharged home. The difference persisted when length
of stay during readmission for up to 90 days after surgery
LDP ODP
(n = 29) (n = 29) P* was included in the analysis. The reduction in hospital stay
did not involve an increase in the duration of surgery or
Tumour size (mm) 33(21) 30(16) 0⋅493
readmission rate.
IPMN 30 (24–39) 39 (22–55) 0⋅748
(n = 8) (n = 5) The laparoscopically treated patients had significantly
Cystic tumour (excluding IPMN) 23 (18–33) 30 (21–49) 0⋅199 less blood loss, although the number of complications
(n = 5) (n = 10) was not reduced. In addition, the significantly higher ASA
Neuroendocrine tumour 25 (11–30) 14 (10–29) 0⋅445 grade in the laparoscopic group, as well as somewhat higher
(n = 7) (n = 6)
age (although not significantly different), did not translate
Adenocarcinoma 35 (24–90) 27 (n.a.) 0⋅667
to a higher complication rate. The significant difference in

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(n = 6) (n = 2)
Pancreatitis (n = 0) (n = 6) – time to functional recovery further supported the obtained
Other 45 (n.a.) (n = 0) – results. Pancreas-specific complications, POPF and PPH,
(n = 3) did not differ significantly between the groups, further
Values are median (i.q.r.). LDP, laparoscopic distal pancreatectomy; OPD, indicating that laparoscopy is a safe approach for distal
open distal pancreatectomy; IPMN, intraductal papillary mucinous neo- pancreatectomy. DGE is a well known complication of
plasia; n.a., not applicable (missing value). *Mann–Whitney U test.
pancreatic surgery, and was encountered more frequently
in the open group in this study, although the difference
The overall complication rate and complications specif- was not significantly different from that in the laparoscopy
ically related to pancreatic surgery were also similar in group. When assessed for only clinically relevant (grade B
the two groups (Table 3). In the laparoscopic group, three and C) DGE, no difference was found.
patients had ultrasound-guided drains placed after surgery The results of the present study are in most aspects sim-
owing to fluid collections in the abdomen, with or without ilar to those of de Rooij and colleagues7 . The present
increased amylase levels, and one patient had both drainage patients were somewhat older and had higher ASA grades,
of the abdomen and endoscopic retrograde cholangiopan- especially in the LDP group, whereas BMI, previous
creatography with placement of a pancreatic duct endo- abdominal surgery and preoperative tumour size were
prosthesis. In the open group, eight patients had severe approximately the same. The differences in duration of
complications, one of whom was treated in the ICU surgery and blood loss may be attributed to the higher
for POPF and respiratory failure. One patient in the proportion of spleen-preserving procedures in the LEOP-
ODP group died, after discharge, 51 days after surgery ARD trial7 , as well as the multicentre nature of that trial,
from a cerebrovascular incident. In addition, four patients which included some centres with a very small number of
underwent abdominal drainage, one patient was treated patients. This is further supported by the larger i.q.r. for
with transgastric drainage of a pancreatic fluid collec- duration of surgery and blood loss in that trial, whereas the
tion, and another had a gastroscopy for pain related to single-centre nature of the present trial accounts for the
food intake. narrow i.q.r. observed for most variables. The main out-
The number of patients with pancreatic adenocarcinoma comes of the studies, overall length of stay and functional
was low in both groups, limiting the possibility of statistical recovery (despite small differences in the definitions used),
analysis for this parameter. However, in the LDP group, are the same, supporting the generalizability of the present
the median number of assessed lymph nodes was 15 (9–18), results. Furthermore, previous non-randomized studies2,3
and four of six patients had an R0 resection with a 1-mm also had similar results, despite variations in the use of
margin. laparoscopy as well as outcomes.
Table 4 shows the histopathological outcomes. A notable difference between this study and that of
de Rooij et al.7 comparing LDP and OPD is the higher
proportion of cystic pancreatic lesions in the present
Discussion
RCT. This may be related to different criteria applied
This randomized trial has demonstrated a shorter hospital for resections of cystic pancreatic lesions and possibly
stay for LDP compared with ODP, confirming earlier expansion of operability criteria, as suggested by higher
published data2,3,7 , even in settings where the hospital stay mean age in the present study population. However, the
after ODP was already short. The shorter hospital stay introduction of laparoscopy per se has not changed the
occurred not only in the hepatopancreatobiliary centre, but surgical indications for cystic pancreatic lesions in the
also included the full hospital stay until the patients were authors’ hospital.

© 2020 The Authors. British Journal of Surgery published by John Wiley & Sons Ltd www.bjs.co.uk BJS 2020; 107: 1281–1288
on behalf of BJS Society Ltd.
Duration of hospital stay after distal pancreatectomy 1287

Some study limitations warrant discussion. The number associated outcome metrics in a universal health care system.
of patients included was not powered to detect differences Pancreatology 2019; 19: 880–887.
in the secondary outcomes. Blinding was not found to 5 van Hilst J, de Rooij T, Bosscha K, Brinkman DJ, van
be practical at the time of study commencement, and Dieren S, Dijkgraaf MG et al.; Dutch Pancreatic Cancer
was therefore not applied. Nevertheless, as the study Group. Laparoscopic versus open pancreatoduodenectomy
for pancreatic or periampullary tumours (LEOPARD-2): a
included patients from only one centre, the perioperative
multicentre, patient-blinded, randomised controlled phase
programme was the same for all patients, both at the
2/3 trial. Lancet Gastroenterol Hepatol 2019; 4: 199–207.
hepatopancreatobiliary centre and at their referral hos-
6 Mehrabi A, Hafezi M, Arvin J, Esmaeilzadeh M, Garoussi C,
pitals. As this laparoscopic group included only patients Emami G et al. A systematic review and meta-analysis of
operated on by a single surgeon in a single centre, the laparoscopic versus open distal pancreatectomy for benign
generalizability and reproducibility of the results is low. and malignant lesions of the pancreas: it’s time to randomize.

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However, previous research2,3,7 , including multicentre and Surgery 2015; 157: 45–55.
nationwide data, supports the findings of the present study. 7 de Rooij T, van Hilst J, van Santvoort H, Boerma D, van den
Furthermore, the study started after almost 40 patients Boezem P, Daams F et al.; Dutch Pancreatic Cancer Group.
had been operated on using the laparoscopic approach, Minimally invasive versus open distal pancreatectomy
which is double the number of patients suggested for the (LEOPARD): a multicenter patient-blinded randomized
learning curve for the procedure17 – 19 . controlled trial. Ann Surg 2019; 269: 2–9.
Owing to the inclusion criteria, many patients with indi- 8 Hartwig W, Vollmer CM, Fingerhut A, Yeo CJ,
cations for extended pancreatic tail resection or simultane- Neoptolemos JP, Adham M et al.; International Study Group
ous resection of other organs were not included. There- on Pancreatic Surgery. Extended pancreatectomy in
fore, the results cannot be applied to advanced tumours pancreatic ductal adenocarcinoma: definition and consensus
of the International Study Group for Pancreatic Surgery
in the body or tail of the pancreas. Because this study
(ISGPS). Surgery 2014; 156: 1–14.
included a limited number of patients with pancreatic duc-
9 Hasselgren K, Halldestam I, Fraser MP, Benjaminsson
tal adenocarcinoma, and these were allocated primarily to
Nyberg P, Gasslander T, Björnsson B. Does the introduction
LDP, statistical analysis of oncological outcomes is of lim- of laparoscopic distal pancreatectomy jeopardize patient
ited value, and no conclusions about the oncological ade- safety and well-being? Scand J Surg 2016; 105: 223–227.
quacy of LDP can be drawn. The ongoing DIPLOMA 10 Björnsson B, Sandström P, Larsson AL, Hjalmarsson C,
trial (ISRCTN44897265; www.e-mips.com) will hopefully Gasslander T. Laparoscopic versus open distal pancreatec-
clarify the role of LDP in the setting of ductal adenocarci- tomy (LAPOP): study protocol for a single center, nonblin-
noma of the pancreas. ded, randomized controlled trial. Trials 2019; 20: 356.
11 Dindo D, Demartines N, Clavien PA. Classification of
Acknowledgements surgical complications: a new proposal with evaluation in a
This study was funded by the Medical Research Council cohort of 6336 patients and results of a survey. Ann Surg
2004; 240: 205–213.
of Southeast Sweden (FORSS), grant nos 567361, 660741
12 Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M,
and 757551.
Adham M et al.; International Study Group on Pancreatic
Disclosure: The authors declare no conflict of interest.
Surgery (ISGPS). The 2016 update of the International
References Study Group (ISGPS) definition and grading of
1 Gagner M, Pomp A, Herrera MF. Early experience with postoperative pancreatic fistula: 11 years after. Surgery 2017;
laparoscopic resections of islet cell tumors. Surgery 1996; 161: 584–591.
120: 1051–1054. 13 Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ,
2 Lof S, Moekotte AL, Al-Sarireh B, Ammori B, Aroori S, Izbicki JR et al. Delayed gastric emptying (DGE) after
Durkin D et al.; Minimally Invasive Liver and Pancreatic pancreatic surgery: a suggested definition by the
Surgery Study Group – UK (MI-LAPS UK). Multicentre International Study Group of Pancreatic Surgery (ISGPS).
observational cohort study of implementation and outcomes Surgery 2007; 142: 761–768.
of laparoscopic distal pancreatectomy. Br J Surg 2019; 106: 14 Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A,
1657–1665. Gouma DJ et al. Postpancreatectomy hemorrhage (PPH): an
3 Søreide K, Olsen F, Nymo LS, Kleive D, Lassen K. A International Study Group of Pancreatic Surgery (ISGPS)
nationwide cohort study of resection rates and short-term definition. Surgery 2007; 142: 20–25.
outcomes in open and laparoscopic distal pancreatectomy. 15 Tingstedt B, Andersson B, Jönsson C, Formichov V, Bratlie
HPB (Oxford) 2019; 21: 669–678. SO, Öhman M et al. First results from the Swedish National
4 Søreide K, Nymo LS, Kleive D, Olsen F, Lassen K. Variation Pancreatic and Periampullary Cancer Registry. HPB (Oxford)
in use of open and laparoscopic distal pancreatectomy and 2019; 21: 34–42.

© 2020 The Authors. British Journal of Surgery published by John Wiley & Sons Ltd www.bjs.co.uk BJS 2020; 107: 1281–1288
on behalf of BJS Society Ltd.
1288 B. Björnsson A. Lindhoff Larsson, C. Hjalmarsson, T. Gasslander and P. Sandström

16 Asbun HJ, Stauffer JA. Laparoscopic approach to distal and 18 Braga M, Ridolfi C, Balzano G, Castoldi R, Pecorelli N, Di
subtotal pancreatectomy: a clockwise technique. Surg Endosc Carlo V. Learning curve for laparoscopic distal
2011; 25: 2643–2649. pancreatectomy in a high-volume hospital. Updates Surg
17 Barrie J, Ammori BJ. Minimally invasive distal 2012; 64: 179–183.
pancreatectomy: a single-center analysis of outcome with 19 Ricci C, Casadei R, Buscemi S, Taffurelli G, D’Ambra M,
experience and systematic review of the literature. Surg Pacilio CA et al. Laparoscopic distal pancreatectomy: what
Laparosc Endosc Percutan Tech 2015; 25: factors are related to the learning curve? Surg Today 2015; 45:
297–302. 50–56.

Editor’s comments

Downloaded from https://academic.oup.com/bjs/article/107/10/1281/6139390 by guest on 08 July 2024

Benefits and boundaries to laparoscopic distal pancreatectomy
The LAPOP trial1 is only the second trial to randomize between open and laparoscopic distal pancreatectomy. The
implementation of laparoscopic distal pancreatectomy has been documented to be rather slow2 and variable3 , despite
several reported short-term benefits over open surgery4 . Shorter time to recovery, less bleeding and shorter hospital
stay feature among the benefits reported across studies. However, the accumulated data stem mainly from retrospective
series, and balanced group comparisons have been lacking. Thus, the LAPOP trial adds to the body of evidence for
laparoscopic distal pancreatectomy, confirming a short-term benefit with a one-day reduction in length of stay at the
treating institution. Also, a reduced total number of hospital days was reported as well as a quicker time to functional
recovery. There were no differences in complications with a 31 and 38 per cent postoperative pancreatic fistula rate
in both arms. The other randomized study (the Dutch multicentre LEOPARD trial), found a similar gain in reduced
length of stay and hence laparoscopy was cost-similar to open distal pancreatectomy5 , but with no differences in quality
of life or perception of cosmesis between the groups after one year.
The LAPOP trial started in a period when little data existed for laparoscopic distal pancreatectomy, and was designed
and run as a single-surgeon laparoscopic arm, which is a limitation. BJS is committed to prioritizing future randomized
trials and studies in this respect to widen the generalizability of results and document the effects on outcomes. Also, the
predominant indication of cystic lesions in LAPOP, several of a smaller size, should be viewed in light of an evolving
understanding for indications for resection of pancreatic cystic lesions. Some lesions may be tempting to resect as low
hanging fruit, but indications should remain the same independent of surgical access. Few patients with cancer were
included, as expected from the uncertainty around oncological issues at the time when the trial was designed. The
debate around the role of minimal access and outcomes in this setting remains unsettled. Despite this, the LAPOP
trial brings controlled data together with the LEOPARD trial to confirm short-term gains with the laparoscopic
approach. The next boundaries to cross will be further safe implementation, generalizability and more widespread
use of laparoscopy, demonstrating similar efficacy for other indications than predominantly smaller cystic lesions and,
for neoplastic disorders, to confirm a non-inferiority in oncological outcomes to open resection.

K. Søreide
Editor, BJS

References
1 Björnsson B, Lindhoff Larsson A, Hjalmarsson C, Gasslander T, Sandström P. Comparison of the duration of hospital stay
after laparoscopic or open distal pancreatectomy: randomized controlled trial. Br J Surg 2020; 107.
2 Lof S, Moekotte AL, Al-Sarireh B, Ammori B, Aroori S, Durkin D et al. Multicentre observational cohort study of
implementation and outcomes of laparoscopic distal pancreatectomy. Br J Surg 2019; 106: 1657–1665.
3 Soreide K, Nymo LS, Kleive D, Olsen F, Lassen K. Variation in use of open and laparoscopic distal pancreatectomy and
associated outcome metrics in a universal health care system. Pancreatology 2019; 19: 880–887.
4 Fingerhut A, Uranues S, Khatkov I, Boni L. Laparoscopic distal pancreatectomy: better than open? Transl Gastroenterol Hepatol
2018; 3: 49.
5 van Hilst J, Strating EA, de Rooij T, Daams F, Festen S, Groot Koerkamp B et al. Costs and quality of life in a randomized trial
comparing minimally invasive and open distal pancreatectomy (LEOPARD trial). Br J Surg 2019; 106: 910–921.

© 2020 The Authors. British Journal of Surgery published by John Wiley & Sons Ltd www.bjs.co.uk BJS 2020; 107: 1281–1288
on behalf of BJS Society Ltd.