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Laparoscopic versus open distal pancreatectomy: a systematic
review of comparative studies
Asri C. Jusoh •Basil J. Ammori
Received: 20 January 2011 / Accepted: 17 October 2011 / Published online: 15 November 2011
ÓSpringer Science+Business Media, LLC 2011
Abstract
Introduction The laparoscopic approach to distal pan-
createctomy (DP) for benign and malignant diseases
appears to offer advantages and is replacing open surgery
in some centers. This review examined the evidence from
published data of comparative studies of laparoscopic
versus open DP.
Methods The Medline and PubMed databases were
searched and relevant English language publications were
systematically retrieved. Data were pooled by two inde-
pendent reviewers. The results shown represent mean.
Results Up to December 2010, 13 comparative studies of
laparoscopic versus open DP were identified of which two
were excluded, leaving 503 and 588 patients respectively
for analysis. The conversion rate was 9.5%. The groups
were comparable for age and sex, whilst open surgery was
associated with significantly higher incidence of malignant
pathology (20.1 vs. 15.0%) and larger tumors (3.9 vs.
3.5 cm) compared with laparoscopic surgery. There were
no differences between the two approaches with regard to
the operative time (220 vs. 208 min), rate of postoperative
pancreatic fistula (16.1 vs. 19.5%), and mortality (0.6 vs.
0.5%). However, the laparoscopic approach was associated
with significantly lower operative blood loss (237 vs.
562 ml), higher spleen preservation rate (37.8 vs. 8%),
lower morbidity (30.5 vs. 38.4%), and shorter postopera-
tive hospital stay (9.1 vs. 14.7 days).
Conclusions The laparoscopic approach to DP offers
advantages over open surgery with lower operative mor-
bidity, higher spleen preservation rate, and shorter hospital
stay; these benefits are particularly observed in patients
with benign disease and borderline malignancy. The
experience with laparoscopic DP for malignant disease
remains limited, and long-term follow-up data are required
to clearly define this role.
Keywords Laparoscopic Distal Pancreatectomy
Open Comparative Tumor
Distal pancreatectomy (DP) is one of the contemporary
applications of advanced laparoscopic surgery, although it
is not yet widely practiced and its optimal techniques and
patient benefits remain to be clarified. The applications of
laparoscopic DP are likely to increase, however, as an
increasing number of premalignant pancreatic neoplasms
are incidentally detected with the expansion of utilization
of cross-sectional imaging of the abdomen for a wide range
of indications [1]. Whilst technically demanding, the lap-
aroscopic approach to DP benefits from the avoidance of a
large incision to access this deep-seated retroperitoneal
organ, an enhanced operative vision and access, a relatively
small specimen and the absence of need for reconstruction.
Several reports of laparoscopic DP have demonstrated
the safety and feasibility of this approach, particularly for
premalignant tumors, with a reasonable postoperative
morbidity, and with potential advantages over open surgery
in terms of hospital stay and time to recovery [1–3]. This
evidence, however, has not been fully tested in the context
of a randomized trial. This systematic review of published
A. C. Jusoh B. J. Ammori
Department of Hepato-Pancreato-Biliary Surgery,
North Manchester General Hospital, Delaunays Road,
Crumpsall, Manchester M8 5RB, UK
B. J. Ammori (&)
School of Biomedicine, The University of Manchester,
Manchester, UK
e-mail: Bammori@btinternet.com
123
Surg Endosc (2012) 26:904–913
DOI 10.1007/s00464-011-2016-3
and Other Interventional Techniques
comparative studies of laparoscopic versus open DP was
designed to appraise critically the claims of such benefits,
and we believe that this is the first systematic review of this
subject in the literature.
Materials and methods
Review strategy
This review employed the Medline and PubMed databases
between 1989 and November 2010 and applied the search
words ‘‘laparoscopic’’ and ‘‘pancreatectomy’’ in combina-
tion. Relevant articles identified by cross-referencing also
were retrieved and reviewed. The review included all the
relevant publications in the English literature. The two
authors independently appraised the data from each series.
Abstracts, letters, reviews, and noncomparative series of
laparoscopic or open DP were excluded.
Outcomes
The clinical outcomes that were analyzed and compared
between the laparoscopic and open approaches to DP
included operative time, estimated blood loss, spleen
preservation rate, postoperative hospital stay, rates of
morbidity and mortality, postoperative pancreatic fistula
(POPF) rate, need for reintervention, and the characteristics
of the resected tumors. The definitions applied for post-
operative pancreatic fistula were noted.
Statistical analysis
The denominator for any outcome measure was the total
number of patients in each series that presented data in
relation to that outcome. The reported results were aver-
aged by weighting for sample size in each study. The
results are presented as mean [±standard deviation (SD)]
or as median (range). Comparisons between the groups
were performed by using the Mann–Whitney Utest for the
not normally distributed parameters, the independent-
samples ttest for normally distributed parameters, and the
v
2
and Fisher’s exact tests for categorical variables. A two-
tailed PB0.05 value was considered to be statistically
significant.
Results
The initial search yielded 256 abstracts. Figure 1demon-
strates a flow chart of the search history that yielded 13
comparative studies of laparoscopic versus open DP pub-
lished between 2006 and December 2010 [4–16]. Two of
these studies were excluded from the analysis for the reasons
described below [7,11], leaving 11 comparative studies of
503 laparoscopic and 588 open resections for analysis.
Quality of the comparative studies and exclusions
from this review
There were no randomized studies. There were shortcom-
ings in the design and reporting of some studies. The
comparative study by Finan et al. [11] was excluded from
this review, because the two surgical groups were imbal-
anced with significantly larger tumors and higher propor-
tion of malignant pathology in the open series, and the
authors did not analyze their results on intention-to-treat
basis but rather inappropriately included the patients con-
verted to open surgery in the open group. The comparative
study by Bruzoni and Sasson [7] also was excluded from
this review, because it included only patients who under-
went spleen-preserving laparoscopic or open DP.
Of the remaining 11 studies that were included in this
review, only that of Baker et al. [12] was prospective
(Table 1), although it did not adopt an intention-to-treat
analysis and excluded patients who were converted to open
DP from the comparative analysis. To overcome the
weaknesses of a retrospective study, a number of authors
matched the laparoscopic and open groups for disease
pathology and often for age and sex [4,10,14,15].
Total number of abstracts
studied (n=256)
Excluded abstracts:
Non comparative studies: 32
Case reports : 45
Not relevant : 114
Non English : 14
Reviews or opinions : 31
Animal studies : 8
(n=243)
Full articles retrieved
(n=13)
Articles that fulfilled the
criteria for analysis:
(n=11)
Two articles excluded [11, 15]
Fig. 1 Flow chart outlining the search history for published reports
of laparoscopic versus open distal pancreatectomy
Surg Endosc (2012) 26:904–913 905
123
Table 1 Details of patients from comparative studies of laparoscopic versus open distal pancreatectomy
Study No. of patients Study design Sex: M, F Age (year)* BMI (kg/m
2
)
Lap
(n=363)
Open
(n=453)
Lap Open Pvalue Lap Open Pvalue Lap Open Pvalue
Velanovich
[4]
15 15 Retrospective, case-matched for
pathology, sex and age
6, 9 NA NA 65 (±14) NA NA NA NA
Tang et al. [5] 9 5 Retrospective, ITT analysis 3, 6 3, 2 0.334 61 (18–79) 68 (35–77) 1.000 NA NA
Teh et al. [6] 12 16 Retrospective, not matched 4, 8 12, 4 0.03 53.4 (23–81) 51.5 (26–75) 0.56 26.4 27.5 0.86
Eom et al.
[10]
31 62 Retrospective, case-matched for
age, sex and pathology
22, 71 NA 46.7 (±16.7) 47.5 (±14.9) 0.821 22.2 (±2.2) 23 (±3.4) 0.233
Kim et al. [8] 93 35 Retrospective, not matched,
probably no ITT analysis
34, 59 16, 19 0.425 52 (±14.7) 52.9 (±11.7) 0.732 23.4 (15.6–47) 23.9 (18.7–27.2) 0.966
Kooby et al.
[14]
142 200 Retrospective, matched, no ITT
analysis (excluded converted
cases from the comparative
analysis)
NA NA NA 59 (±13) 58.4 (±14.3) 0.71 27.7 (±6.3) 27 (±6.4) 0.2
Matsumoto
et al. [9]
14 19 Retrospective, not matched 7, 7 7, 12 0.5 58.6 (±17.6) 63.2 (±13.2) 0.31 NA NA
Baker et al.
[12]
27 85 Prospective, non-randomised, no
ITT analysis (excluded the
converted case from analysis)
9, 18 39, 46 0.23 59.2 (±3.2) 59.3 (±1.6) 0.99 NA NA
Nakamura
et al. [13]
20 16 Retrospective, not matched, no
ITT analysis (excluded the
converted case from analysis)
6,14 8, 8 0.31 53.5 (±18.6) 61.5 (±20.6) 0.23 23.4 (±2.9) 21.3 (±4.2) 0.079
Vijan et al.
[15]
100 100 Retrospective, matched, no ITT
analysis (excluded the converted
cases from analysis)
60, 40 50, 50 0.16 59 (±17.3) 58.6 (±15.2) 0.85 27.5 (±5.2) 27.9 (±5) 0.44
Aly et al.
[16]
40 35 Retrospective, not matched, ITT
analysis
14, 26 24, 11 0.004 47.0 (±16.0) 52.0 (±16.0) 0.2 21 (±3) 21 (±3) 0.9
NA not available, ITT intention-to-treat
* Data shown represent mean (±SD) or median (range)
906 Surg Endosc (2012) 26:904–913
123
Patients’ characteristics
The 11 comparative studies of this review included 503
laparoscopic and 588 open resections. Table 1illustrates
the design of the comparative studies and the demographic
characteristics of the patients. Overall, there were no sig-
nificant differences between the two groups with regard to
age, gender, and body mass index.
Outcomes
Data on operative and the postoperative outcomes that
were reported in the 11 studies are listed in Tables 2and 3
respectively. Table 4lists the pathological findings, and
Table 5summarises the overall results.
Operative outcomes
Conversion to open surgery
Two reports failed to declare the conversion rate to open
DP [8,10]. Amongst the remaining nine series, the overall
(range) conversion rate was 9.5% (3.7–20%). The com-
monest reasons for conversion were bleeding [4,6,14–16],
poor exposure [9], intra-abdominal adhesions [15], retro-
peritoneal adhesions secondary to malignancy [4]or
chronic pancreatitis [6], and failure to progress [14]. All
three conversions in Velanovich series were in patients
with pancreatic adenocarcinoma [4]. The hand-assisted
laparoscopic approach was employed in 2–67% of patients
in five [5,6,13–15] of the 11 studies.
Operating time
The operating time for laparoscopic DP was not routinely
defined by authors, except for Kim et al. [8] who defined it
as time taken from skin incision for first trocar insertion to
the time of skin closure of the last port wound. None of the
reports defined the operating time for open DP. The oper-
ating time was reported in ten studies; overall, no signifi-
cant difference in the operating time was found between
the laparoscopic and open approaches (Table 5).
Intraoperative blood loss
Intraoperative blood loss was not reported in one study [4],
and the method used to measure it was not given in five
other studies. Kim et al. [8] reported the reduction of
haemoglobin level before and after surgery, whereas Eom
et al. [10] reported the number of patient who required
transfusion intraoperatively. When the results from four
studies that reported blood loss in milliliters [5,6,9,12]
were pooled, the intraoperative blood loss was significantly
lower in the laparoscopic group (Table 5).
Preservation of the spleen
Some surgeons either never preserved the spleen despite
performing the surgery (laparoscopic or open) exclusively
for benign disease [4] or scarcely preserved it (\3%) [11].
Others preserved the spleen in selected laparoscopic cases
but not with open surgery [5,9]. Amongst those who
preserved the spleen, the preservation rate ranged between
2 and 55.5% with laparoscopic DP and 2.7 and 8% with
open DP. Overall, the spleen preservation rate was signif-
icantly higher with the laparoscopic approach (Table 5).
The impact of further operative efforts to preserve the
spleen during laparoscopic DP on operating time compared
with when the spleen was sacrificed was only examined by
Eom et al. [10] who reported that splenic preservation
significantly prolonged the operating time [194 (±53) vs.
251 (±42) min, P=0.02]; the authors did not report the
spleen preservation rate during open DP.
Postoperative outcomes
Operative morbidity
The range of operative morbidity in ten studies was 7–40%
for laparoscopic DP and 0–57% for open DP, whereas Teh
et al. [6] reported number of complication events. Whereas
Vijan et al. [15] defined morbidity as that occurred within
30 days after surgery, others did not clearly define the
duration after surgery within which complications were
included, e.g., in-hospital or 30-day morbidity. Overall, the
laparoscopic approach was shown to have significantly
lower morbidity rate than open surgery (Table 5).
Postoperative pancreatic fistula
The postoperative pancreatic fistula (POPF) rate range was
0–26% after laparoscopic DP and 0–32% after open
resection. However, the definitions of POPF varied widely
between reports. The International Study Group of Pan-
creatic Fistula (ISGPF) based their definition of POPF [17]
on drain amylase content greater than three times the serum
level after postoperative day 3 was introduced in 2005, and
therefore predated all the studies included in this review.
Nonetheless, only four studies [12,13,15,16] applied the
ISGPF definition. Surprisingly, Nakamura et al. [13] had
no POPF in laparoscopic group.
On the other hand, Eom et al. [10] reported 9.7% POPF
that was defined as drainage exceeding 30 ml of fluid with
an amylase level exceeding 600 U/dl on or after postop-
erative week 1 and therefore might have underestimated its
Surg Endosc (2012) 26:904–913 907
123
Table 2 Operative outcomes of comparative studies of laparoscopic versus open distal pancreatectomy
Study Conversion: no. (%) Operating time (min)* Estimated blood loss (ml)* Spleen preservation: No. (%)
Lap Open Pvalue Lap Open Pvalue Lap Open Pvalue
Velanovich (2006) [4] 3 (20) NA NA NA NA NA NA 0 0 1.000
Tang et al. (2007) [5] 0 180 (120–250) 210 (120–260) 0.411 100 (120–250) 450 (200–2200) 0.021 5 (55.5) 0 0.086
Teh et al. (2007) [6] 2 (16.7) 212 (60–360) 278 (180–420) 0.05 193 (25–800) 609 (150–2000) 0.012 5 (41.7) 1 (6.3) 0.057
Eom et al. (2008) [10] NA 217 (±55.8) 194.8 (±63.7) 0.093 Blood transfusion: 0.261 13 (41.9) NA NA
1 patient 7 patients
Kim et al. (2008) [8] NA 195 (82–453) 190 (88–482) 0.905 Hb ;1.1 (±1.1) mg/dl Hb ;1.1 (±1.3) mg/dl 0.652 38 (40.8) 2 (5.7) \0.001
Kooby et al. (2008) [14] 20 (12.6) 230 (±97) 216 (±100) 0.28 357 (±497) 588 (±591) \0.001 43 (30) 24 (12) \0.001
Matsumoto et al. (2008) [9] 1 (7.1) 290.7 (±53.2) 213.8 (±84.6) 0.002 247.1 (±227.4) 400.3 (±423.5) 0.29 1 (7.1) 0 1.000
Baker et al. (2009) [12] 1 (3.7) 236 (±15.8) 253.2 (±31.7) 0.63 219.4 (±30.6) 612.6 (±80.7) \0.01 NA NA NA
Nakamura et al. (2009) [13] 1 (4.7) 308.4 (±124.6) 281.5 (±83.3) 0.46 249.0 (±239.8) 714.1 (±650.4) 0.005 7 (35) 5 (31) [0.99
Vijan et al. (2010) [15] 4 (4) 214 (±NA) 208 (±NA) 0.5 171 (±NA) 519 (±NA) \0.001 25 (25) NA NA
Aly et al. (2010) [16] 4 (10) 342 (±133) 250 (±98) 0.000 363 (±549) 606 (±602) 0.001 13 (32) 3 (8) 0.01
NA not available
* Data shown represent mean (±SD) or median (range)
Table 3 Postoperative outcomes of comparative studies of laparoscopic versus open distal pancreatectomy
Study Complications: no. (%) Pancreatic fistula: no. (%) Hospital stay (days)* Mortality: no. (%)
Lap Open Pvalue Lap Open Pvalue Lap Open Pvalue Lap Open Pvalue
Velanovich (2006) [4] 3 (20) 4 (27) 1.000 2 (13) 2 (13) 1.000 5 (3–9) 8 (6–23) 0.020 NA NA NA
Tang et al. (2007) [5] 3 (33.3) 0 (0.0) 0.346 2 (22.2) 0 (0) 0.505 7 (4–53) 11 (8–17) 0.255 NA NA NA
Teh et al. (2007) [6] 2 events 9 events 0.030 1 (8.3) 1 (6.2) 0.83 6.2 (3–16) 10.6 (7–19) 0.01 0 0 NS
Eom et al. (2008) [10] 11 (35.5) 15 (24.2) 0.253 3 (9.7) 4 (6.5) 0.58 11.5 (±4.1) 13.5 (±4.9) 0.049 0 0 NS
Kim et al. (2008) [8] 23 (24.7) 11 (29) 0.880 8 (8.6) 5 (14.3) 0.316 10 (5–36) 16 (8–65) \0.001 0 0 NS
Kooby et al. (2008) [14] 57 (40) 113 (57) 0.003 37 (26.0) 64 (32.0) 0.28 5.9 (±3.8) 9.0 (±6.0) \0.001 0 1 (1) 0.4
Matsumoto et al. (2008) [9] 1 (7) 4 (21) 0.620 0 2 (10.5) 0.496 12.9 (±4.8) 23.8 (±11.8) 0.004 0 0 NS
Baker et al. (2009) [12] 10 (37) 30 (35.1) 0.82 6 (22) 12 (14) 0.38 4.0 (±0.3) 8.6 (±0.7) \0.01 0 1 (2) 0.16
Nakamura et al. (2009) [13] 0 3 0.078 0 2 (12.5) 0.19 10.0 (±2.6) 25.8 (±8.8) \0.0001 0 0
Vijan et al. (2010) [15] 34 (34) 29 (29) 0.45 17 (17) 17 (17) [0.99 6.1 (±2.4) 8.6 (±5.9) \0.001 3 (3) 1 (1) 0.62
Aly et al. (2010) [16] 8 (20) 11 (31) 0.3 5 (12) 6 (17) 0.5 22 (±16) 27 (±13) 0.009 0 0
NA not available, NS not significant
* Data shown represent mean (±SD) or median (range)
908 Surg Endosc (2012) 26:904–913
123
true incidence. Similarly, with a definition of drainage of
amylase-rich fluid ([5,000 U/L) beyond postoperative day
7, Matsumoto et al. [9] reported no POPF after laparo-
scopic DP and a low POPF rate of 10.5% with open sur-
gery. Kim et al. [8] also adopted the high-threshold for
definition proposed by Sarr et al. [18] of drain amylase five
times greater than the serum level and a drain amount of
more than 30 ml 5 days or longer after surgery, and
reported an overall POPF rate of 10.2%.
Allowing for these variations in definition, there were
no significant differences in the overall POPF rates
between the laparoscopic and open approaches.
Operative mortality
With the exception of two studies that did not report
operative mortality [4,5], the overall safety of DP was
reflected in 0.6% mortality with the laparoscopic approach
and 0.5% (range 0–2%) mortality with open surgery
(Table 5). Vijan et al. defined mortality as in-hospital or
30-day mortality [15] and reported three deaths (3%) in the
laparoscopic DP group (pulmonary embolus, n=2; pan-
creatic leak, n=1) and one death in the open DP group
(pulmonary embolus). Two further deaths were reported
after open DP in other series (acute myocardial infarction
[12], unreported cause [14]).
Postoperative analgesia
Four studies reported the postoperative analgesic usage
[5,8,9,16] and detected differences in favour of laparo-
scopic surgery. These differences were significant in terms
of the number of analgesics consumed [9] and their dura-
tion [16].
Return of bowel function
Laparoscopic surgery was associated with significantly
shorter times to first flatus [9] return to oral intake [9],
return of bowel movement [8], and resumption of oral diet
[8], as well as significantly greater proportion of patients
achieving adequate oral intake within 72 h of surgery [6]
compared with open resections. On the other hand, Aly
et al. [16] found the days to first flatus, water, and meal
intake comparable.
Postoperative hospital stay
All the reports except for that by Tang et al. [5] detected a
significantly shorter postoperative hospital stay with lapa-
roscopic surgery compared with open, and this was
reflected in the overall result (Table 5). The rather long
Table 4 Pathological characteristics of resected tumours
Study Tumor size (cm)* Neuroendocrine Cystic neoplasms and IPMN Adenocarcinoma Malignant pathology Chronic pancreatitis
Lap Open Pvalue Lap Open Lap Open Lap Open Lap Open Lap Open
Velanovich (2006) [4] NA NA NA 2 (13) NA
à
8 (53) NA
à
3 (20) NA
à
NA NA
à
2 (13) NA
à
Tang et al. (2007) [5] NA NA NA 1 (11.1) 0 5 (55.5) 3 (60) 0 0 0 0 1 (11.1) 1 (20)
Teh et al. (2007) [6] 3.4 (±NA) 3.4 (±NA) 0.09 9 (42) 9 (56) 3 (25) 3 (34) 0 0 0 0 1 (2) 1 (8)
Eom et al. (2008) [10]4(±2.3) 6.2 (±4.1) 0.006 2 (6.5) 6 (9.6) 26 (83) 51 (82) NA NA 3 (9.7) 4 (6.5) 0 0
Kim et al. (2008) [8] 3.4 (0.9–13) 3 (1–13) 0.19 7 (7.5) 1 (2.9) 71 (76) 20 (57.1) 0 0 0 0 10 (10.8) 6 (17.1)
Kooby et al. (2008) [14] 3.2 (±1.7) 3.3 (±1.7) 0.60 NA NA 82 (58) 107 (54) NA NA 54 (38) 84 (43) 5 (4) 7 (4)
Matsumoto et al. (2008) [9]3(±2.7) 3.4 (±1.7) 0.120 4 (28.5) 1 (5.2) 10 (71.4) 18 (94.7) 0 0 0 0 0 0
Baker et al. (2009) [12] 3.8 (±0.4) 4 (±0.4) 0.66 NA NA NA NA 1 (4.1) 18 (21.1) 8 (30.1) 25 (29.0) 3 (11) 22 (26)
Nakamura et al. (2009) [13] 4.8 (±3.3) 4.1 (±2.1) 0.515 4 (20) 2 (12.5) 12 (60) 10 (62.5) 0 0 2 (10.0) 1 (6.2) 0 3 (18.7)
Vijan et al. (2010) [15] 3.3 (±1.9) 4 (±2.9) 0.02 27 (27) 30 (30) 49 (49) 43 (43) 17 (17) 19 (19) 6 (6) 4 (4) 1 (1) 4 (4)
Aly et al. (2010) [16]3(±2) 4 (±2) 0.06 9 (12) 2 (2.6) 23 (30.6) 20 (26.7) 0 0 0 0 8 (10.6) 12 (16)
* Data shown represent mean (±SD) or median (range), the remaining data represent number of patients (%)
àThe author presented pathology results for the whole group of open experience (n=41) rather than of the matched cases (n=15) drawn from it
NA not available, IPMN intraductal papillary mutinous neoplasm
Surg Endosc (2012) 26:904–913 909
123
postoperative hospital stay reported by Matsumoto et al. [9]
Nakamura et al. [13] and Aly et al. [16] with either of the
surgical approaches compared with others reflected, as the
authors explained, cultural differences.
Return to normal activity
Velanovich [4] retrospectively obtained information from
patients and reported that laparoscopic patients returned to
normal activity in 3 weeks (range 2–7) compared with
6 weeks (range 4–10) for open patients (P=0.03).
Cost
Eom et al. [10] reported that the hospital cost for laparo-
scopic resection was significantly higher than for open sur-
gery [4,884 (±1,845) vs. 3,401 (±1,248) US$, P\0.001],
whereas Kim et al. [8] reported no difference in cost [527
(±164) vs. 550 (±319) 10,000 Won, P=0.582].
Pathology
Table 4illustrates the major, but not all, the pathological
classifications of the resected lesions. Five comparative
studies included patients with benign but not malignant
diseases [5,6,8,9,16]. Amongst the five studies that
included malignant pathology [10,12–15], the frequencies
of resections for malignant pathology were comparable
between the two approaches (Table 5). Cystic neoplasms
and neuroendocrine tumors represented the majority of
overall resections with no notable differences between the
two surgical approaches.
Whereas the laparoscopically resected tumors appeared
relatively smaller than those resected at laparotomy, this
difference was statistically significant in only two reports
[10,15] (Table 4). Overall, the tumor size was significantly
smaller in the laparoscopic series compared with the open
(Table 5).
Discussion
This review evaluated the current best available evidence
for the role of laparoscopic versus open approaches to DP.
There are no randomized trials but a number of compara-
tive studies, some of which matched the two approaches for
patients’ demographics and disease characteristics. There
were some shortcomings in the design and reporting of
some of the comparative studies with higher incidence of
malignancy and larger tumor size in some of the open
series. However, the evidence points to advantages for the
laparoscopic approach in patients with benign or borderline
malignant disease. The laparoscopic approach was associ-
ated with significantly lower operative blood loss, lower
morbidity, and shorter hospital stay. The practice of lapa-
roscopy in performing DP for malignant disease varied
amongst institutions; although no clear disadvantages were
identified, long-term follow-up data were not available.
When considering the design of the comparative trials,
we acknowledge that the relative infrequency of pancreatic
diseases that require DP renders the conduction of a ran-
domized trial with sufficient sample size and statistical
power very difficult to achieve unless it is set within a
multicentre multinational design. To minimize the bias of
Table 5 Summary of results of
comparative studies of
laparoscopic versus open distal
pancreatectomy
Data are numbers with
percentages in parentheses
unless otherwise indicated
* Series that included both
benign and malignant disease in
the laparoscopic and in the open
approaches [14,16–19]
Laparoscopic series Open series Pvalue
No. of
patients
available for
analysis
Result No. of
patients
available for
analysis
Result
Total no. of patients 503 588
Conversion 379 36 (9.5)
Operating time, mean (min) 488 220.4 573 208.6 NS
Intraoperative blood loss,
mean (ml)
364 237.4 476 562.4 \0.001
Spleen preservation 476 180 (37.8) 441 35 (8) \0.001
Operative morbidity 491 150 (30.5) 572 220 (38.4) 0.007
Postoperative pancreatic fistula 503 81 (16.1) 588 115 (19.5) 0.154
Operative mortality 479 3 (0.6) 568 3 (0.5) 1.000
Postoperative hospital stay,
mean (days)
503 9.1 588 14.7 \0.001
Malignant pathology 488 73 (15) 573 118 (20.1) 0.02
320* 71 (22.2)* 463* 119 (25.7)* 0.271*
Tumor size, mean (cm) 479 3.5 568 3.9 0.001
910 Surg Endosc (2012) 26:904–913
123
comparative nonrandomized and often retrospective stud-
ies, some authors matched both groups according to age,
gender, and pathology [4,10,14,15]. In this review, we
excluded the report by Finan et al. [11] who had signifi-
cantly larger tumors with greater proportion of malignancy
in the open series and who did not adhere to the principles
of intention-to-treat but rather analyzed conversions to
open DP amongst the open surgery group. A further
shortcoming of some of the comparative studies included
in this review is the nonadherence to the principles of
intention-to-treat analysis as the laparoscopic cases that
were converted to open DP were excluded from the anal-
ysis [12–15]. In general, because all of the studies were
nonrandomized, the evidence available can only be con-
sidered as level III or IV evidence and the recommenda-
tions issued at grade C [19].
The safety of the laparoscopic approach to DP is well
demonstrated in these comparative studies with lower
operative blood loss and lower morbidity than that of open
surgery and no mortality. The lower morbidity is in part
related to the avoidance of the disproportionately long
abdominal incision of open surgery. Taking into account
the varied definitions applied by different authors for
POPF, it is worth noting that laparoscopic surgery did not
increase the incidence of this complication compared with
open surgery.
The rates of POPF varied considerably amongst sur-
geons, and this is probably attributable to the array of def-
initions employed rather than the surgical technique with
the highest rates being observed amongst series that strictly
adhered to the ISGPF definition [17] of drain amylase
content greater than three times the serum level after post-
operative day 3. The only measure that has been shown to
reduce POPF is that of direct identification and suturing of
the transected pancreatic duct [20], although a meta-anal-
ysis suggested stapler closure to be superior, albeit statis-
tically short of significance [21]. Whilst Abu Hilal et al. [22]
suggested that oversewing of the stapled pancreatic stump
reduced the incidence of POPF compared with stapler
division alone (nine vs. 50%), the groups were rather
small and unmatched (11 and six patients respectively).
Fortunately, the firm and fibrotic remnant in patients with
chronic pancreatitis protects these immune-compromised
patients [23] (who often require a concomitant splenectomy
with its added risk of infective complications [24]) against
POPF.
A healthy conversion rate from laparoscopic to open DP
of 9.5% is observed with uncontrolled bleeding, poor
exposure, inflammatory adhesions, lack of progress, and the
incidental detection of malignancy being the commonest
reasons. It is perhaps not surprising to observe that lapa-
roscopic surgery was associated with significantly lower
blood loss compared with open surgery. The magnified
views of laparoscopy and the surgeons’ heightened intol-
erance for bleeding with this approach may have contrib-
uted, although pathological characteristics, such as smaller
tumors and lower incidence of malignancy also might have
played a role. Nonetheless, the significant reduction in
blood loss was clearly evident amongst comparative series
that excluded malignancy [5,6]. It is interesting to note that
the reduction in blood loss was achieved with the laparo-
scopic approach despite the significantly higher rate of the
technically demanding spleen-preserving DP.
Some might argue that the higher rate of spleen preser-
vation observed with laparoscopic DP might have been
related to the higher prevalence of benign disease among
patients subjected to this approach; however, there is no
sufficient explanation. In this review, the spleen preserva-
tion rate was 23% higher with laparoscopy (33.3 vs. 10.5%),
whereas the incidence of malignancy was *7% greater
with open surgery (26 vs. 19.3%). The superior operative
exposure and the reduced blood loss would undoubtedly
have played a role. Preservation of the spleen in patients
with benign or low-grade malignancy is a physiologically
desired end point and requires commitment from the sur-
geon, because it is technically more demanding and has
been shown to increase operative time significantly by
*1h[10]. Preservation of the spleen can be accomplished
through preservation of the splenic artery and vein, pres-
ervation of the splenic artery and short gastric vessels with
sacrifice of the splenic vein, or preservation of the short
gastric vessels and arcade with sacrifice of both splenic
vessels (Warshaw technique), although the latter has at least
a 10% incidence of subsequent splenic infarction and need
for splenectomy [7]. On the other hand, incidence of splenic
infarction following the Warshaw technique from open
series of DP by Rodriquez et al. was much lower at 1.6%
(1/60 patients) [25]. There is a suggestion that retrograde
DP (tail-to-body) might technically facilitate splenic pres-
ervation compared with prograde (body-to-tail) resection
[26]. Concurrent splenectomy has been shown to increase
perioperative infective complications after DP [24] as well
as after gastrectomy [27] and colectomy [28].
This review confirms that the laparoscopic approach was
associated with a significantly shorter hospital stay com-
pared with open surgery. This may be attributed to gains in
terms of operative morbidity, severity of pain, and anal-
gesic requirements [5,8,9], as well as the shorter time
taken to resumption of oral intake [6,9] and return of
bowel function [8]. The shorter hospital stay appears to be
paralleled by a more rapid recuperation after discharge
from the hospital with shorter time to return to normal
activity following laparoscopic surgery [4].
It is evident that the role of laparoscopic DP for malig-
nancy remains a controversial issue; some surgeons treat
all patients with preoperative [5] or intraoperative [13]
Surg Endosc (2012) 26:904–913 911
123
diagnosis of malignancy by open surgery, whereas others
performed laparoscopic resection if judged technically fea-
sible [12,14,15]. Malignancy was one of the reasons for
need to convert from laparoscopic to open surgery, either for
technical difficulties [4] or on principle [13]. It is useful to
note, however, that comparative studies that included fairly
similar proportions of malignant resections in the laparo-
scopic and open groups found no evidence of increased
operative morbidity with laparoscopy [10,14,15].
The current evidence regarding the oncologic appro-
priateness of the laparoscopic approach to DP in the
resection of malignant disease lacks long-term data.
However, the disease clearance achieved by the laparo-
scopic and open approaches seems to be comparable. In
their multicenter comparative analysis of laparoscopic
versus open DP for pancreatic ductal adenocarcinoma,
Kooby et al. found no difference in the rates of positive
resection margin (34 vs. 26%, P=0.61), the number of
nodes examined (13.8 ±8.4 vs. 12.5 ±8.5, P=0.47),
and overall survival (median, 16 vs. 16 months, P=0.71);
their multivariate analysis found that the method of
resection did not have an impact on the resection margin
[29]. In another report of laparoscopic DP in 27 patients
with malignancy, Fernandez-Cruz et al. were able to
achieve R0 resection in 90% of ductal adenocarcinoma
patients with mean lymph node count of 14.5 ±3[30].
In conclusion, the laparoscopic approach to DP offers
clear benefits in terms of reduction of operative blood loss,
increase in rate of preservation of the spleen in suitable
cases, enhancement of recovery, and reduction in postop-
erative hospital stay particularly in patients with benign
and borderline malignant pathology (level II evidence).
The laparoscopic approach to DP for these patients there-
fore should be considered the ‘‘gold standard’’ within
institutions that have this expertise (grade C recommen-
dation). Laparoscopic DP in selected patients with malig-
nancy is feasible and has no disadvantages in terms of
operative morbidity and recovery; however, the contro-
versy regarding this application of laparoscopy will require
long-term oncologic follow-up data to resolve.
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