REVIEW

Laparoscopic pancreaticoduodenectomy: a systematicliterature review

Ugo Boggi • Gabriella Amorese • Fabio Vistoli • Fabio Caniglia • Nelide De Lio •

Vittorio Perrone • Linda Barbarello • Mario Belluomini • Stefano Signori •

Franco Mosca

Received: 22 December 2013 / Accepted: 31 May 2014

� Springer Science+Business Media New York 2014

Abstract

Background Laparoscopic pancreaticoduodenectomy

(LPD) is gaining momentum, but there is still uncertainty

regarding its safety, reproducibility, and oncologic appro-

priateness. This review assesses the current status of LPD.

Methods Our literature review was conducted in Pubmed.

Articles written in English containing five or more LPD

were selected.

Results Twenty-five articles matched the review criteria.

Out of a total of 746 LPD, 341 were reported between 1997

and 2011 and 405 (54.2 %) between 2012 and June 1,

2013. Pure laparoscopy (PL) was used in 386 patients

(51.7 %), robotic assistance (RA) in 234 (31.3 %), lapa-

roscopic assistance (LA) in 121 (16.2 %), and hand assis-

tance in 5 (0.6 %). PL was associated with shorter

operative time, reduced blood loss, and lower rate of

pancreatic fistula (vs LA and RA). LA was associated with

shorter operative time (vs RA), but with higher blood loss

and increased incidence of pancreatic fistula (vs PL and

RA). Conversion to open surgery was required in 64 LPD

(9.1 %). Operative time averaged 464.3 min (338–710)

and estimated blood 320.7 mL (74–642). Cumulative

morbidity was 41.2 %, and pancreatic fistula was reported

in 22.3 % of patients (4.5–52.3 %). Mean length of hos-

pital stay was 13.6 days (7–23), showing geographic var-

iability (21.9 days in Europe, 13.0 days in Asia, and

9.4 days in the US). Operative mortality was 1.9 %,

including one intraoperative death. No difference was

noted in conversion rate, incidence of pancreatic fistula,

morbidity, and mortality when comparing results from

larger (C30 LPD) and smaller (B29 LPD) series. Pathology

demonstrated ductal adenocarcinoma in 30.6 % of the

specimens, other malignant tumors in 51.7 %, and benign

tumor/disease in 17.5 %. The mean number of lymph

nodes examined was 14.4 (7–32), and the rate of micro-

scopically positive tumor margin was 4.4 %.

Conclusions In selected patients, operated on by expert

laparoscopic pancreatic surgeons, LPD is feasible and safe.

Keywords Pancreaticoduodenectomy � Laparoscopy �Robot � Da Vinci

First described in 1994 [1], laparoscopic pancreaticoduo-

denectomy (LPD) is eventually gaining momentum at

specialized centers. Acceptance was probably slowed by

both the inherent technical limitations of laparoscopy and

the need for advanced endoscopic skills which, until

recently, were not acquired during the training of pancreas

surgeons [2]. Successful application of laparoscopy to

other complex abdominal operations [3–5], availability of

newer technologies, such as the da Vinci surgical system�

(Intuitive Surgical, Sunnyvale, California, USA) [6], and

surgeons’ motivation to pursue innovation and accept

challenge [7] have all contributed to increase popularity

and acceptance of LPD.

Four techniques are currently employed for LPD: pure

laparoscopy (PL), hand-assisted (HA) laparoscopy,

U. Boggi (&) � F. Vistoli � F. Caniglia � N. De Lio �V. Perrone � L. Barbarello � M. Belluomini �S. Signori � F. Mosca

Division of General and Transplant Surgery, Azienda

Ospedaliero Universitaria Pisana, Via Paradisa 2, 56124 Pisa,

Italy

e-mail: u.boggi@med.unipi.it

G. Amorese

Division of General and Vascular Anesthesia and Intensive Care,

Pisa University Hospital, Pisa, Italy

123

Surg Endosc

DOI 10.1007/s00464-014-3670-z

and Other Interventional Techniques

laparoscopic-assisted (LA) surgery, and robotic-assisted

(RA) laparoscopy. No comparative study between the four

techniques is available.

For this article, we reviewed the English literature to

provide a comprehensive understanding of the current

status of LPD, focusing on technical challenges and spe-

cific complications of minimally invasive approaches.

Materials and methods

Definitions and surgical techniques

In PL, both resection and reconstruction are carried out

laparoscopically [8–19]. HA laparoscopy adds a hand port

to facilitate the progress of the operation [17–19]. In LA,

surgery resection is carried out laparoscopically and

digestive reconstruction is performed under direct vision

through a small mini-laparotomy incision [14–16, 20–24].

In RA laparoscopy, the da Vinci surgical system� is

employed either for the entire operation [25–30] or for

dissection of the uncinate process/posterior margin and

digestive reconstruction [11, 31, 32].

Literature review

A literature search was performed using Pubmed database

using the key words ‘‘laparoscopy,’’ or ‘‘laparoscopic,’’ or

‘‘hand-assisted,’’ or ‘‘robotic,’’ or ‘‘da vinci’’ combined

with ‘‘pancreaticoduodenectomy,’’ or ‘‘Whipple proce-

dure,’’ or ‘‘pancreatic resection.’’ The final search was

completed by June 1, 2013. Relevant articles identified by

cross-referencing were also retrieved and reviewed. Arti-

cles written in English containing more than 5 LPD were

selected. Review articles, not reporting original data, were

excluded. In case of multiple publications from the same

institution, only the more informative was considered, in

order to exclude data overlap.

Two authors (UB and GA) independently reviewed all

the retrieved studies that met the inclusion and exclusion

criteria. Discrepancies between the two reviewers were

resolved by discussion and consensus.

The following variables were extracted from each study:

number of patients, number of ports, optic port site, side of

‘‘fourth’’ robotic arm (for robotic-assisted operations),

energy device used for dissection, energy device used for

pancreatic neck section, technique employed to seal gas-

troduodenal artery, specimen extraction site, use of drains,

management of pancreatic stump, preference for gastric

resection or pylorus preservation, technique of gastric/

duodenal anastomosis, route of anastomotic gastric/duo-

denal jejunal loop, conversion rate, operative time, blood

loss, length of hospital stay, overall morbidity, overall

mortality, pancreatic fistula rate, type of pancreatic disease

treated, number of examined lymph nodes, and rate of

margin negative resection.

Whenever applicable, a weighted average (WA) was

used to express the statistical sum of all the means for the

different variables [33].

Statistical analysis

The chi-square or Fisher’s exact test was used to compare

categorical variables between groups, as appropriate. The

Student’s unpaired t test was used to compare continuous

variables. A p value \0.05 was considered statistically

significant.

Results

Twenty-five articles, reporting on 746 LPD, were included

in this review (Fig. 1). The first series of LPD was pub-

lished in 1997, the second one in 2006. Twelve articles

were published between 1997 and 2011, reporting on 341

LPD (45.7 %), while 13 articles were published between

January 1, 2012, and June 1, 2013, reporting on 405 LPD.

Six articles, reporting on 225 LPD, were published during

the first 5 months of 2013 (Fig. 2). LPD were reported by

Institutions from the USA, South Korea, Italy, India,

China, Japan, France, and UK in order of decreasing fre-

quency (Fig. 3).

Surgical technique

Eighteen authors used one technique, while seven used two

techniques. Three hundred and eighty-six patients were

operated on by PL (51.7 %), 234 by RA (31.3 %), 121 by

LA (16.2 %), and 5 by HA (0.6 %) (Fig. 4). After the first

reported series of RA LPD in 2010 [32], 567 LPD were

reported of which 234 (41.2 %) employed RA, either

through the entire operation (n = 138; 58.9 %) or to dis-

sect the posterior margin and to perform digestive recon-

struction (n = 96; 41.0 %) (Table 1).

Most authors report the use of 5 (n = 12; 52.1 %) or 6

ports (n = 7; 30.4 %). Lee et al. [24] used 5 or 6 ports,

Pugliese et al. [14] and Lei et al. [19] 4 ports, Zeh et al.

[31] and Palanivelu et al. [12] 7 ports, and Kendrick and

Cusati [11] 6 or 7 ports. The position of the optic port was

specified in 19 articles (n = 584; 78.2 %), being umbilical

in 10 (n = 244; 41.7 %), right pararectal in 3 (n = 194;

33.2 %), right paraumbilical in 3 (n = 93; 15.9 %), infra-

umbilical in 2 (n = 31; 5.3 %) and supra-umbilical in 1

(n = 22; 3.7 %). In the nine articles reporting on 234 RA

LPD, the position of the ‘‘fourth’’ robotic arm was specified

in 6 (n = 188; 80.3 %), being located on the right side in 4

Surg Endosc

123

articles (n = 134; 71.2 %), and on the left side in 2

(n = 54; 28.7 %) (Table 2).

Details on energy device used for dissection were pro-

vided in 22 articles (n = 678; 90.8 %). In 14 articles, a

single device was employed, while in 8, two devices were

used. Ultrasonic shears alone were employed in 10 articles

(n = 393; 57.9 %), and radiofrequency shears alone in 4

(n = 137; 20.2 %). Ultrasonic and radiofrequency shears

were used in 6 articles (n = 103; 15.1 %), bipolar elec-

trocautery and ultrasonic shears in 1 article (n = 35;

5.1 %), and electrocautery and ultrasonic shears in 1 article

(n = 10; 1.4 %) (Table 2).

Details on the method used to seal the gastroduodenal

artery were provided in 17 articles (n = 502; 67.2 %).

Clips alone were used in 7 articles (274; 54.5 %), and

ligature alone in 3 articles (n = 100; 19.9 %). Ligature

plus vascular stapler or suture ligature (n = 50; 9.9 %),

clips plus suture ligature (n = 35; 6.9 %), stapler (n = 14;

2.7 %), radiofrequency shears (n = 11; 2.1 %), clips or

stapler (n = 10; 1.9 %), and ligature plus clips (n = 8;

1.5 %) were described in 1 article each. When limiting this

analysis to the 6 articles in which RA was used also for

early dissection (n = 168), the technique used to seal the

gastroduodenal artery was specified in 4 articles (n = 144;

85.7 %). Ligature was employed in 94 LPD (65.2 %), and

clips alone in 50 (34.7 %) (Table 2).

Details on the device used to divide the pancreatic neck

site were provided in 21 articles (n = 652; 87.3 %). The

use of ultrasonic shears was reported in 14 articles

(n = 365; 55.9 %), and the use of electrocautery in 3

articles (n = 104; 15.9 %). The use of stapler or ultrasonic

shears (n = 100; 15.3 %), electrocautery or ultrasonic

shears (n = 65; 9.9 %), stapler (n = 12; 1.8 %), and

Fig. 1 Flowchart of systematic review

Fig. 2 Number of studies published yearly

Fig. 3 Number of laparoscopic pancreaticoduodenectomies by

country

Fig. 4 Number of laparoscopic pancreaticoduodenectomies by sur-

gical technique

Surg Endosc

123

radiofrequency shears (n = 6; 0.9 %) was reported in 1

article each (Table 2).

Details on specimen extraction site were provided in 23

articles (n = 725; 97.1 %). In 7 articles, the specimen was

extracted through an umbilical incision (n = 306; 42.2 %),

in 3 articles each through a suprapubic (n = 114; 15.7 %),

subxiphoid (n = 109; 15.0 %), or supra-umbilical (n = 36;

4.9 %) incision. In 2 articles, the specimen was delivered

through a right lower quadrant incision (n = 64; 8.8 %),

while in the remaining 4 articles through an infra-umbilical

incision (n = 65; 8.9 %), an enlarged trocar site (n = 16;

2.2 %), at infra-umbilical or suprapubic level (n = 8;

1.1 %), or the extraction site was indicated as variable

(n = 7; 0.9 %) (Table 2).

Details on use of drains were provided in 18 articles

(n = 628; 86.6 %). Only Kendrick and Cusati declared to

systematically avoid drains (n = 65; 8.9 %) [11] (Table 2).

Information on management of pancreatic stump was

available from 23 articles (n = 682; 94.0 %). In 20 arti-

cles, a single technique was employed. Overall, the

majority of pancreatic remnants were drained into the

jejunum (n = 573; 84.0 %). Pancreaticogastrostomy was

employed in 67 patients (9.8 %) and duct occlusion in 47

(6.8 %). Additional details on management of pancreatic

stump were reported less precisely. With this limitation,

further analysis shows that most pancreatic anastomoses

were stented either routinely or selectively (n = 269/369;

72.8 %) and made up in a double layer (n = 492/543;

90.6 %) of interrupted sutures (n = 347/465; 74.6 %)

(Table 3).

Pylorus preservation (n = 350/636; 55.0 %) was

employed more frequently than resection of gastric antrum

(n = 286/636; 44.9 %). Among 21 authors clearly

describing their policy, 6 elected to always preserve the

pylorus (n = 262/636; 41.1 %), 8 to always resect the

gastric antrum (n = 113/636; 17.7 %), and 7 employed

both techniques (n = 261/636; 41.0 %). In most patients,

the jejunal loop used for duodenal or gastric anastomosis

followed an antecolic route (n = 306/401; 76.3 %). The

retromesenteric (n = 54/401; 13.4 %) or retrocolic

(n = 41/401; 10.2 %) routes were employed less fre-

quently. Hand-sewing (n = 491/566; 86.7 %) was adopted

more frequently than stapling (n = 75/566; 13.2 %) for

construction of gastro- or duodenal anastomosis. Stapling

was employed only for gastrojejunostomy (Table 4).

Outcome

Information on conversion to open surgery was reported in

23 articles (n = 699; 93.6 %). Overall, 64 LPD were

converted to open surgery (9.1 %). Reasons for conversion

were: tumor adherence/invasion into superior mesenteric/

portal vein (n = 19) [8, 9, 11, 15, 16, 30, 31], portal vein

bleeding (n = 10) [8, 10, 14, 22, 27, 32], obesity (n = 7)

[10, 16, 30, 31], pancreatitis (n = 4) [16, 28, 30], limited

working space (n = 4) [18], positive margins (n = 3) [29,

30], robotic system malfunction (n = 1) [30], hypercapnia

(n = 1) [30], tumor adhesion to hepatic hilum (n = 1)

[15], hepatic artery injury (n = 1) [16], or unspecified

reasons (n = 12) [14, 24, 30, 32]. One patient underwent

planned conversion for digestive reconstruction in the early

experience by Kendrick and Cusati [11]. Several authors

reported decreasing conversion rates as a result of their

learning curve [11, 16, 30, 31].

Information on intra- and postoperative outcome mea-

sures is presented in Table 5.

Table 1 Articles reporting on five or more laparoscopic

pancreaticoduodenectomies

First author

[Ref.]

Country Publication

year

Technique Cases

Boggi [25] Italy 2013 RA 34

Lee [24] South

Korea

2013 LA 42

Lei [19] China 2013 PL, HA 11

Corcione [8] Italy 2013 PL 22

Kim [16] South

Korea

2013 PL, LA 100

Zhan [26] China 2013 RA 16

Asbun [9] US 2012 PL 42

Chalikonda [27] US 2012 RA 30

Kuroki [20] Japan 2012 LA 20

Lai [28] China 2012 RA 20

Nakamura [21] Japan 2012 LA 12

Suzuki [22] Japan 2012 LA 6

Zeh [31] US 2012 RA 50

Zhou [29] China 2011 RA 8

Ammori [17] UK 2011 PL, HA 7

Zureikat [10] US 2011 PL 14

Giulianotti [30] Italy/US 2010 RA 60

Kendrick [11] US 2010 PL, RA 65

Narula [32] US 2010 RA 8

Cho [23] Japan 2009 LA 15

Palanivelu [12] India 2009 PL 75

Gumbs [13] US 2008 PL 35

Pugliese [14] Italy 2008 PL, LA 19

Dulucq [15] France 2006 PL, LA 25

Gagner [18] US 1997 PL, HA 10

746

PL pure laparoscopic pancreaticoduodenectomy, HA hand-assisted

pancreaticoduodenectomy, LA laparoscopy-assisted pancreaticoduo-

denectomy, RA robotic-assisted pancreaticoduodenectomy, UK Uni-

ted Kingdom, US United States

Surg Endosc

123

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Surg Endosc

123

Mean operative time, reported in 24 articles (n = 734;

98.3 %), ranged from 338 to 710 min, with a WA of

464.3 min.

Mean volume of intraoperative blood loss, reported in

19 articles (n = 575; 77.0 %), ranged from 74 to 642 mL,

with a WA of 320.7 mL.

Mean length of hospital stay, reported in 22 articles

(n = 679; 91.0 %), ranged from 7 to 23 days, with a WA

of 13.6 days. Interestingly enough, WA of length of hos-

pital stay was 21.9 days for 143 LPD performed in Europe,

13.0 days for 293 LPD performed in Asia, and 9.4 days for

243 LPD performed in North America. These figures do

not completely match with reported incidence of postop-

erative complications, pancreatic fistula and postoperative

mortality from the three continents (Table 6).

Information on incidence of postoperative complications

was included in 20 articles (n = 611; 81.9 %). Morbidity

ranged between 18.1 and 64.2 %. Overall, 252 patients

developed postoperative complications giving a total

morbidity rate of 41.2 %. Information on pancreatic fistula,

although not always recorded according to standardized

methodology, was reported in 21 articles (n = 681;

91.2 %). Incidence of pancreatic fistula ranged between 4.5

and 52.3 %. Overall, 152 patients developed a pancreatic

fistula, giving a total pancreatic fistula rate of 22.3 %.

When limiting this analysis to 403 LPD, reported in 13

articles [9, 10, 14, 16, 17, 20, 22–25, 27, 30, 31], in which

pancreatic fistula was scored according to the international

definition [34], the overall incidence of pancreatic fistula

was 24.8 % (100/403). Fifty-seven patients developed

grade A pancreatic fistula (14.1 %), 29 grade B pancreatic

fistula (7.1 %), and 14 grade C pancreatic fistula (3.4 %).

Information on postoperative mortality was available in

23 articles (n = 720; 96.5 %). Mortality rate ranged

between 0 and 7.1 %. A total of 14 postoperative deaths

were reported giving an overall postoperative mortality rate

of 1.9 %. Intraoperative mortality occurred in one patient,

who died because of massive bleeding from portal vein

injury, despite conversion to open surgery [27].

Pure laparoscopy versus laparoscopic-assisted surgery

versus robotic-assisted laparoscopy

HA was not considered in this analysis due to the small

number of reported operations. Further, only series

reporting on one surgical technique were analyzed because

data were reported cumulatively when multiple techniques

were employed at a single Institution. A total of 188 PL, 95

LA surgery, and 226 RA laparoscopy were available for

comparison (Table 7). The three techniques achieved

similar results respect to overall morbidity and mortality.

PL, however, was associated with shorter operative time,

reduced estimated blood loss, and lower rate of pancreaticTa

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Surg Endosc

123

Table 3 Management of

pancreatic stump in

laparoscopic

pancreaticoduodenectomy

DL double layer, DO duct

occlusion, D-t-M duct-to-

mucosa, E-to-E end-to-end, E-

to-S end-to-side, PD pancreatic

duct, PG pancreatogastrostomy,

PJ pancreatojejunostomy, RS

running suture

* The authors used either

interrupted or continuous

sutures posteriorly and

interrupted sutures anteriorly

First author

[Ref.]

Duct management technique Stent Suture

Technique

PJ PG DO RS DL

Boggi [25] 34 (100 %)

[D-to-M or E-to-S]

0 0 NA No Yes

Lee [24] 0 42 (100 %) 0 NA NA NA

Lei [19] 11 (100 %) 0 0 Yes (10/11) No Yes

Corcione [8] 13 (59 %)

[10 E-to-E; 3 D-to-M]

3 (13.6 %) 6 (27.2 %) NA NA NA

Kim [16] 90 (100 %)

[E-to-E normal PD; D-to-M

enlarged PD]

0 0 NA NA Yes

Zhan [26] NA NA NA NA NA NA

Asbun [9] 42 (100 %)

[D-to-M]

0 0 Yes No Yes

Chalikonda [27] 30 (100 %)

[D-to-M]

0 0 Yes No Yes

Kuroki [20] 20 (100 %)

[D-to-M]

0 0 NA NA Yes

Lai [28] 20 (100 %)

[D-to-M (PD [ 3 mm).

Dunking (PD B 3 mm)]

0 0 Selectively NA Yes

Nakamura [21] 12 (100 %)

[Kakita’s technique]

0 0 Yes No Yes

Suzuki [22] 3 (50 %)

[D-to-M]

3 (50 %) 0 Yes

[In PJ]

No Yes

Zeh [31] 50 (100 %)

[D-to-M]

0 0 Yes No Yes

Zhou [29] 8 (100 %)

[E-to-S]

0 0 NA NA Yes

Ammori [17] 7 (100 %)

[E-to-S or D-to-M]

0 0 Yes * No

Zureikat [10] 14 (100 %)

[D-to-M]

0 0 NA Yes Yes

Giulianotti [30] 0 19 (31.6 %) 41 (68.3 %) NA Yes NA

Kendrick [11] 62 (100 %)

[D-to-M]

0 0 Yes No Yes

Narula [32] 8 (100 %)

[D-to-M]

0 0 NA No Yes

Cho [23] 15 (100 %)

[E-to-S]

0 0 NA NA NA

Palanivelu [12] 75 (100 %)

[E-to-S]

0 0 No No Yes

Gumbs [13] NA NA NA NA NA NA

Pugliese [14] 19 (100 %)

[E-to-S]

0 0 Yes Yes No

Dulucq [15] 25 (100 %) 0 0 No Yes No

Gagner [18] 10 (100 %) 0 0 Yes No Yes

Surg Endosc

123

fistula. LA surgery required shorter operative time, as

compared to RA laparoscopy, but entailed higher estimated

blood loss and increased the incidence of pancreatic fistula.

Large versus smaller series

Ten institutions reported on 30 or more LPD (n = 533),

and 15 institutions on 29 or fewer LPD (n = 213)

(Table 8).

Smaller series employed LA surgery more frequently

reported longer operative time and greater estimated blood

loss. No difference, however, was noted in conversion rate,

incidence of pancreatic fistula, morbidity, and mortality.

Pathology

Information on tumor type was provided in 21 articles.

Data were available from 632 patients (84.7 %), mostly

because some authors did not provide information on

tumor type for patients converted to open surgery. All

authors but Kuroki et al. [20] operated at least one ductal

adenocarcinoma. Overall, there were 194 pancreatic ductal

adenocarcinomas (30.6 %), 327 other malignant or bor-

derline tumors (51.7 %), and 111 benign lesions (17.5 %).

Data on examined lymph nodes were reported in 19

articles (n = 635; 85.1 %). The mean number of lymph

nodes examined per specimen ranged from 7 to 32, with a

WA of 14.4 lymph nodes.

Margin status and tumor type were described in 16

articles reporting on 467 patients (62.6 %) operated on for

malignant or borderline tumors. In 11 articles (n = 240;

51.3 %), the R0 rate was 100 %, while in the remaining 5

articles (n = 227; 48.6 %) it ranged from 73.3 to 97.2 %.

Overall, there were 21 patients with microscopically

positive margins out of 467 PD specimens (4.4 %)

(Table 9).

Discussion

In 1994, Gagner and Pomp showed that LPD was feasible

[1], but nearly 30 years later this operation has not been

Table 4 Management of gastric/duodenal stump in laparoscopic pancreaticoduodenectomy

First author [Ref.] Antrectomy Loop route Anastomotic technique

Yes No Retromesenteric Retrocolic Antecolic Hand-sewn Stapled

Boggi [25] NA NA 34 (100 %) 0 0 34 (100 %) 0

Lee [24] 0 42 (100 %) 0 0 42 (100 %) 42 (100 %) 0

Lei [19] 11 (100 %) 0 NA NA NA 0 11 (100 %)

Corcione [8] 22 (100 %) 0 0 22 (100 %) 0 NA NA

Kim [16] 0 90 (100 %) NA NA NA 90 (100 %) 0

Zhan [26] NA NA NA NA NA 16 (100 %) 0

Asbun [9] 3 (7.1 %) 39 (92.8 %) 0 0 42 (100 %) 39 (92.8 %) 3 (7.1 %)

Chalikonda [27] 0 30 (100 %) 0 0 30 (100 %) 30 (100 %) 0

Kuroki [20] 4 (20 %) 16 (80 %) 0 0 20 (100 %) NA NA

Lai [28] 20 (100 %) 0 20 (100 %) 0 0 NA NA

Nakamura [21] NA NA NA NA NA NA NA

Suzuki [22] 6 (100 %) 0 0 0 6 (100 %) 6 (100 %) 0

Zeh [31] 36 (72 %) 14 (28 %) NA NA NA NA NA

Zhou [29] 5 (62.5 %) 3 (37.5 %) NA NA NA NA NA

Ammori [17] 7 (100 %) 0 0 0 7 (100 %) 7 (100 %) 0

Zureikat [10] 14 (100 %) 0 0 0 14 (100 %) 0 14 (100 %)

Giulianotti [30] 50 (83.3 %) 10 (16.6 %) NA NA NA 60 (100 %) 0

Kendrick [11] 61 (98.3 %) 1 (1.6 %) 0 0 62 (100 %) 62 (100 %) 0

Narula [32] 8 (100 %) 0 0 0 8(100 %) 0 8 (100 %)

Cho [23] 0 15 (100 %) NA NA NA 15 (100 %) 0

Palanivelu [12] 0 75 (100 %) 0 0 75 (100 %) 75 (100 %) 0

Gumbs [13] NA NA NA NA NA NA NA

Pugliese [14] 14 (73.6 %) 5 (26.3 %) 0 19 (100 %) 0 5 (26.3 %) 14 (73.6 %)

Dulucq [15] 25 (100 %) 0 NA NA NA 0 25 (100 %)

Gagner [18] 0 10 (100 %) NA NA NA 10 (100 %) 0

NA not available

Surg Endosc

123

included in the standard therapeutic armamentarium of

pancreatic surgeons yet. This delay is probably explained

by the intrinsic technical limitations of laparoscopy, and

the lack of agreed standards for subspecialty training in

advanced laparoscopic techniques [2].

As shown in this review, the scenario is quickly

evolving. Seven hundred and forty-six LPD were published

in series reporting on a minimum of five patients, and other

operations, not included in this review, were published as

case reports or smaller series [35–40]. Interestingly

enough, the number of LPD published between January 1,

2012, and June 1, 2013 exceeds that of LPD published in

the previous 15 years. These figures, if on one hand, show

that LPD is quickly maturing into an acceptable surgical

technique, at least in some specialty centers and/or in the

hands of gifted laparoscopic surgeons, on the other, should

be carefully interpreted and selectively translated into

standard surgical practice. Indeed, pursuing LPD in the

occasional patient, or in small series, could entail high

complication rates and/or excessively long learning curve

Table 5 Outcome laparoscopic pancreaticoduodenectomy

First author [Ref.] Conversion Operative time (min) Blood loss (mL) LOS (days) Morbidity Pancreatic fistula Mortality

Boggi [25] 0 597 (420–960) 220 (150–400) 23 (10–86) 55.8 % 38.2 % 2.9 %

Lee [24] 7.1 % 404.4 ± 30.5 374.5 ± 176.9 17.1 ± 9.2 35.7 % 52.3 % 2.3 %

Lei [19] 0 473.8 (300 1106.0 ± 52.67 18.1 ± 5.9 18.1 % 9.1 % 0

Corcione [8] 9.1 % 392 (327–570) NA 23 (12–35) 63.6 % 27.3 % 4.5 %

Kim [16] 4.7 % 7.9 h (5.0–13.5) NA 11.5 (7–40) 43.8 % 25.7 % 0.9 %

Zhan [26] 0 479.7 ± 111.5 633.8 ± 264.5 23 ± 7 37.5 % 6.2 % NA

Asbun* [9] 16.9 % 541 ± 88 195 ± 136 8 ± 3.2 47.1 % 16.7 % 5.6 %

Chalikonda [27] 10.0 % 476 (363–727) 485 (50–3,500) 9.79 30.0 % 6.6 % 3.3 %

Kuroki [20] 0 656.6 ± 191.4 376.6 ± 291.4 NA NA 45.0 % 0

Lai [28] 5.0 % 491.5 ± 94 247 (50–889) 13.7 ± 6.1 50.0 % 35.0 % 0

Nakamura [21] NA NA NA NA NA NA 0

Suzuki [22] 16.6 % 581 (507–817) 475 (415–3,860) 23 (11–36) 33.3 % 33.3 % 0

Zeh [31] 16.0 % 568 (536–629) 350 (150–625) 10 (8–13) 58.0 % 22.0 % 2.0 %

Zhou [29] 0 718 ± 186 153 ± 43 16.4 ± 4.1 25.0 % 25.0 % 0

Ammori [17] 0 628.6 (420–720) 350 (300–500) 11.1 (6–23) 28.6 % 14.3 % 0

Zureikat [10] 14.2 % 456 (334–583) 300 (150–1,300) 8 (5–28) 64.2 % 35.7 % 7.1 %

Giulianotti [30] 18.3 % 421 (240–660) 394 (80–1,500) 22 (5–85) NA 31.6 % 3.3 %

Kendrick [11] 4.6 % 368 (258–608) 240 (30–1,200) 7 (4–6) 41.9 % 17.7 % 1.6 %

Narula [32] 37.5 % 7 h (6–8.5) NA 9.6 NA NA 0

Cho [23] 0 338 ± 48 445 ± 384 16.4 ± 3.7 26.6 % 13.3 % 0

Palanivelu [12] 0 357 (270–650) 74 (35–410) 8.2 (6–42) 26.6 % 6.6 % 1.3 %

Gumbs [13] NA 360 300 NA NA NA 0

Pugliese [14] 31.5 % 461 ± 90 NA 18 (13–37) 36.8 % 15.7 % 0

Dulucq [15] 12.0 % 287 ± 39 107 ± 48 16.2 ± 2.7 31.8 % 4.5 % 4.5 %

Gagner [18] 40.0 % 8.5 h (5.5–12) NA 22.3 (7–62) 30.0 % NA NA

* Includes 9 total pancreatectomies

Table 6 Relationship between mean length of hospital stay and reported incidence of pancreatic fistula, postoperative morbidity, and post-

operative mortality

Continent Pancreatic fistula Morbidity Mortality Mean LOS

(days)n./total % n./total % n./total %

Europe 35/143 24.4 50/107 46.7 5/143 3.4 21.9

North America 40/225 17.7 97/211 45.9 6/233 2.5 9.4

Asia 68/293 23.2 105/293 35.8 3/277 1.0 13.0

143/661 21.6 252/611 41.2 14/653 2.1 13.6

Surg Endosc

123

[41, 42]. State-of-the-art equipment is also necessary since,

especially in a formidable operation like LPD, technical

choices should reflect surgeon preference and not adapta-

tion to limited resource availability. Perhaps the latter issue

is one of the reasons accounting for the patchy geograph-

ical origin of published series, with most LPD reported

from the US, followed by Asian and European countries.

Certainly, the da Vinci system is not evenly available

across the world [43].

Regarding surgical techniques, PL was prevalent fol-

lowed by RA, LA, and HA. The most striking result was

the very limited adoption of HA (0.6 %). HA is typically

felt to increase safety in operations requiring complex

dissections around large vessels [44–46], but location of

the pancreatic head makes it necessary to place the hand-

assisted incision in the right subcostal area or in the lower

right abdominal quadrant [18]. A small incision in these

locations cannot be easily used for digestive reconstruc-

tions. It is reasonable to assume that surgeons able to deal

with complex intracorporeal digestive reconstructions do

not routinely require to have one of their hands inside

during dissection. HA, however, could still be employed to

allow tumor palpation and/or to deal with difficult opera-

tive conditions [18].

LA surgery is also used infrequently (16.2 %), possibly

because keeping the length of working incision within the

limits of minimal invasive surgery (\10 cm?) is not always

possible, especially in western countries where patients are

often overweight or obese. LA surgery can be more con-

veniently employed in lean patients to facilitate digestive

reconstructions, especially at the beginning of an individual

or institutional learning curve.

RA laparoscopy (31.3 %) was used less frequently than

PL (51.7 %). RA laparoscopy is known to improve both

overall surgeon dexterity [47] and non-dominant hand

performance [48, 49], as well as reducing the need for

extensive laparoscopic training [50]. These improvements

are expected to facilitate difficult dissections in deep and

narrow space, such as dissection of the uncinate process,

and fine intracorporeal suturing. On practical grounds,

however, RA laparoscopy in LPD has not reached the

anticipated level of diffusion. Possible explanations include

the fact that pioneer surgeons were often experienced la-

paroscopists, that costs of RA laparoscopy remain high

[25], and that the da Vinci Surgical System� needs to be

refined. The most obvious weaknesses of current robotic

system are lack of haptic feedback [51], risk of system

malfunction [30], possibility of arm collision [51], inability

to reposition the patient once the robot is docked [51], need

for a second experienced surgeon at the table [52], intri-

cacy of instrument exchange disrupting the flow of the

Table 7 Comparison of

surgical techniques for LPD

* t test unpaired, ^ Fisher exact

test

PL

(n = 188)

LA

(n = 95)

RA

(n = 226)

p

PL vs LA PL vs RA LA vs RA

WA of operative

time (min)

410.1 465.9 508.2 0.0001* 0.0001* 0.0004*

(n = 188) (n = 83) (n = 226)

WA of EBL (mL) 171.3 395.0 346.6 0.0001* 0.0001* 0.02*

(n = 166) (n = 83) (n = 218)

Pancreatic fistula (n, %) 23 (15.0 %) 35 (42.2 %) 55 (25.2 %) 0.0001^ 0.02^ 0.005^

(n = 153) (n = 83) (n = 218)

Morbidity (n, %) 61 (39.9 %) 21 (33.3 %) 94 (43.1 %) NS^ NS^ NS^

(n = 153) (n = 63) (n = 218)

Mortality (n, %) 5 (2.7 %) 1 (1.1 %) 5 (2.4 %) NS^ NS^ NS^

(n = 188) (n = 95) (n = 210)

Table 8 Comparison of large vs smaller series

Large series

(n = 533)

Smaller series

(n = 213)

p

Technique (n, %)

PL 299 (56.0 %) 87 (40.8 %) 0.0005*

RA 182 (34.1 %) 52 (24.4 %)

HA 0 5 (2.3 %)

LA 52 (9.7 %) 69 (32.3 %)

WA of operative

time (min.)

447.73 467.42 0.0092^

(n = 533) (n = 533)

WA of blood loss (mL) 274.22 386.29 0.0001^

(n = 433) (n = 142)

Conversion (%) 40 (8.0 %) 22 (10.9 %) NS�(n = 498) (n = 142)

Morbidity (%) 183 (41.7 %) 69 (39.8 %) NS�(n = 438) (n = 173)

Pancreatic fistula (%) 117 (23.4 %) 40 (21.8 %) NS�(n = 498) (n = 183)

Mortality (%) 11 (2.0 %) 3 (1.6 %) NS�(n = 533) (n = 187)

* Chi squared, ^ t test unpaired, � Fisher exact test

Surg Endosc

123

operation [25], and the limited access to the patient by the

anesthesia team in case of exsanguinating hemorrhage [53]

or extubation [54]. Further, the advantages of RA may be

difficult to demonstrate, in the lack of large prospective

data, if technically successful PD can be completed using

conventional laparoscopic techniques. Despite these limi-

tations, everyone who has had the opportunity to test the da

Vinci Surgical System� recognizes that it enhances sur-

geon dexterity in laparoscopy. In some instances, one could

even feel that a given surgical maneuver is easier while

using RA laparoscopy than in open surgery. Although no

technology can surrogate medical knowledge and surgical

expertise, RA laparoscopy could be employed more widely

in the future, especially when technical improvements will

surpass the limitations of current robotic system.

Based on this review, ‘‘standard’’ LPD is currently

carried out by PL, using 5 or 6 trocars. The patient is

placed supine, often with parted legs, in a reverse Tren-

delenburg’s position. The use of ultrasonic shears is pre-

valent among energy devices, while clips and/or ligature

are preferred to seal the gastroduodenal artery. The speci-

men is often extracted through an umbilical or peri-

umbilical incision, and drains are left near the pancreatic

anastomosis. When RA laparoscopy is employed, the so-

called ‘‘fourth’’ robotic arm is more often placed to the

right of the patient, being operated by the left hand of the

surgeon at the console.

The most evident variation of LPD from established

open techniques is probably the method used to divide the

pancreatic neck. In open surgery, sharp division of the

pancreatic neck is advised to preserve blood supply to the

resection margin [55]. Bleeding is in part prevented by

placing stay sutures at the superior an inferior border of the

pancreatic neck, occluding the segmental pancreatic

Table 9 Main pathology

parameters in laparoscopic

pancreaticoduodenectomy

NA not available

First author

[Ref.]

Tumor type Lymph nodes R0

PDAC Potentially malignant

tumors

Benign

tumors

Boggi [25] 5 (14.7 %) 21 (61.7 %) 8 (23.5 %) 32 (15–76) 100 %

Lee [24] 1 (2.3 %) 39 (92.8 %) 2 (4.7 %) 16 100 %

Lei [19] 5 (45.4 %) 4 (36.3 %) 2 (18.1 %) NA 100 %

Corcione [8] 11 (50.0 %) 11 (50.0 %) 0 15 (14–20) 100 %

Kim [16] 7 (7.0 % %) 60 (60.0 %) 33 (33.0 %) 13 (7–34) 100 %

Zhan [26] NA NA NA NA 100 %

Asbun [9] NA NA NA 23.44 ± 10.1 94.9 %

Chalikonda [27] 14 (46.6 %) 4 (13.3 %) 12 (40.0 %) 13.2 (1–37) 100 %

Kuroki [20] 0 20 (100 %) 0 NA NA

Lai [28] 7 (35.0 %) 8 (40.0 %) 5 (25.0 %) 10 ± 6 73.3 %

Nakamura [21] NA NA NA NA NA

Suzuki [22] 4 (66.6 %) 2 (33.3 %) 0 18 (16–27) 100 %

Zeh [31] 14 (28.0 %) 23 (46.0 %) 13 (26.0 %) 17 ± 7 89.1 %

Zhou [29] 1 (12.5 %) 7 (87.5 %) 0 NA 100 %

Ammori [17] 5 (71.4 %) 1 (14.2 %) 1 (14.2 %) 20.8 (11–32) NA

Zureikat [10] 8 (57.1 %) 4 (28.5 %) 2 (14.2 %) 18.5 (12–31) 100 %

Giulianotti [30] 27 (45.0 %) 19 (31.6 %) 14 (23.3 %) 21 (5–37) Italy

14 (12–45) USA

89.1 %

Kendrick [11] 31 (50.0 %) 26 (41.9 %) 5 (8.0 %) 15 (6–31) 89.0 %

Narula [32] 1 (20 %) 0 4 (80 %) 16 NA

Cho [23] 4 (26.6 %) 10 (66.6 %) 1 (6.6 %) 18.5 ± 5.9 100 %

Palanivelu [12] 23 (30.6 %) 49 (65.3 %) 3 (4.0 %) 14 (8–22) 97.2 %

Gumbs [13] NA NA NA NA NA

Pugliese [14] 11 (57.8 %) 7 (36.8 %) 1 (5.2 %) 13.0 (4–22) 100 %

Dulucq [15] 11 (50.0 %) 8 (36.3 %) 3 (13.6 %) NA 100 %

Gagner [18] 4 (40.0 %) 4 (40.0 %) 2 (20.0 %) 7 (3–14) NA

Surg Endosc

123

arteries running in those locations, and in part arrested by

individually suturing spurting bleeders while noting the

position of the main pancreatic duct [55]. Sharp division of

pancreatic neck in LPD is unpractical because of difficult

control of ensuing bleeding. A dry cut surface is preferable,

but requires the use of energy devices. Available systems

are effective, but all entail varying degrees of lateral

thermal spread and collateral tissue injury [56–58]. This

review shows that most authors rely on the harmonic

scalpel to accomplish this key step of PD [9, 11–20, 23, 27,

29, 30, 32]. Should this method be eventually proven to be

safe and effective, the paradigm of sharp division of the

pancreatic neck during PD could be revisited. For the

moment, it should be noted that division of the pancreatic

neck during LPD requires adaptation from the well-estab-

lished technique used in open PD. Further, the results of

LPD in terms of pancreatic fistula could be influenced by

the device used to divide the pancreatic neck.

Pancreaticojejunostomy is by far the most common

technique used to manage the pancreatic remnant in LPD.

In most patients, a stent is placed in the main pancreatic

duct and the anastomosis is constructed using interrupted

sutures.

Pylorus preservation and resection of gastric antrum

were reported in similar percentages with six authors

always pursuing gastric preservation, eight authors always

preferring partial gastrectomy, and seven employing both

techniques. The jejunal loop more often reaches the duo-

denum or the stomach following an antecolic route, and the

anastomosis is stapled only in some of the patients

undergoing gastric resection.

The reported rates of morbidity and mortality,

although possibly underestimated because of selection

and publication biases, show that well-trained surgeons

can safely perform LPD. Reasons for conversion to open

surgery show that tumor adhesion to the mesenteric-

portal vein is a major issue in LPD, including RA lap-

aroscopy. Twenty-nine operations were converted to

open surgery because of overt tumor adhesion/infiltration

into peri-pancreatic vessels (n = 19) or bleeding from

venous injury (n = 10). One intraoperative death occur-

red as a result of portal vein injury despite prompt

conversion to open surgery [27]. Alike in laparoscopic

major hepatectomy [59], a low threshold to conversion

should be maintained and conversion to open should be

considered prudent surgical practice rather than technical

failure.

Average operative time for LPD is between 7 and 8 h,

clearly exceeding that of the open operation. Excluding all

considerations on utilization effectiveness of operating

room time, and related costs, experience with other lapa-

roscopic operations, such as colectomy, shows that pro-

longed operative time entails increased postoperative

morbidity and mortality [60–62]. Prolonged operative time

is associated with higher postoperative morbidity also in

general surgery [62], and open PD is no exception [63].

However, while in open surgery, prolonged operative time

usually reflects difficult dissection and is associated to

increased blood loss and need for blood transfusions [64],

in LPD additional time is required mostly because dissec-

tion must proceed very carefully to avoid major bleeding,

which may be difficult to control laparoscopically. Blood

loss is indeed reduced in LPD, and, in general, fewer

patients require blood transfusions after LPD as compared

to case-matched open PD [65]. Reducing operative time of

LPD is, however, desirable, to optimize the use of oper-

ating room time and allows patients with reduced physio-

logic reserve to safely undergo this operation.

Length of hospital stay varied markedly in reported

series being quite short in US institutions, intermediate in

Asian institutions, and quite long in European institutions.

Since length of hospital stay does not seem to reflect only

the reported incidence and severity of postoperative com-

plications, it reasonable to assume that cultural and orga-

nizational issues account at least for some of these

differences [30]. Unfortunately, information on readmis-

sion was sparse and insufficient to attempt a correlation

with initial length of hospital stay.

Overall, postoperative complications and pancreatic

fistula occurred in percentages similar to those expected in

open PD. However, reliable conclusions cannot be drawn

based on currently available information because results

were not always collected and reported according to stan-

dardized criteria. In particular, regarding pancreatic fistula,

it should be considered that a relevant proportion of

patients undergoing LPD were operated on because of peri-

ampullary malignancy or benign disease. In this setting, the

pancreas is expected to be soft and the pancreatic duct

small, increasing the incidence of pancreatic fistula [66].

Postoperative mortality ranged between 0 and 7.1 %,

with a mean of 1.9 %. Although it is possible that some

deaths were missed, especially in small series that have not

been published yet, these figures show that LPD is rea-

sonably safe, in appropriate hands.

Regarding oncologic outcome, information obtained

from this review are yet inconclusive since the main

objective of most analyzed articles was to show that LPD

was feasible and safe. Pathology information has not been

always collected according to standardized methodology,

especially regarding margin status [67, 68], and could be

biased by the initial patient selection favoring lower grade

tumors and usually avoiding borderline resectable cancers

[69]. With these limitations, the number of lymph nodes

retrieved during LPD and the margin status seem to be

equivalent to historical data on open PD. Actually, there

are few studies comparing open and LPD [8, 20, 23, 27, 29,

Surg Endosc

123

31] further suggesting that LPD is equivalent to open PD as

a cancer operation, in properly selected patients. Confir-

mation of this crucial information can only be obtained in a

prospectively designed study using strict methodology and

recruiting a large number of patients. Until this evidence is

achieved, LPD in the setting of pancreatic cancer should be

pursued with caution.

In conclusion, available information shows that LPD is

feasible in well-selected patients. Standardization of out-

come measures would greatly facilitate inter-institutional

comparison and data pooling. The international registry,

recently implemented by the Association for Endoscopic

Surgery and other interventional techniques, is a first

attempt in this direction (http://www.eaes.eu/activities/

registries/laparoscopic-pancreatoduodenectomy.aspx).

Probably, the many pending questions concerning LPD,

including economic sustainability, will not have convinc-

ing answers until specifically designed prospective studies,

including randomized comparisons with the open opera-

tion, will be available.

Disclosures Ugo Boggi, Gabriella Amorese, Fabio Vistoli, Fabio

Caniglia, Nelide De Lio, Vittorio Perrone, Linda Barbarello, Mario

Belluomini, Stefano Signori and Franco Mosca have no conflicts of

interest or financial ties to disclose.

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