Surg Endosc DOI 10.1007/s00464-014-3670-z
and Other Interventional Techniques
REVIEW
Laparoscopic pancreaticoduodenectomy: a systematic literature 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 Ó 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 appropriateness. 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 %), laparoscopic assistance (LA) in 121 (16.2 %), and hand assistance 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
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: [email protected] G. Amorese Division of General and Vascular Anesthesia and Intensive Care, Pisa University Hospital, Pisa, Italy
in 22.3 % of patients (4.5–52.3 %). Mean length of hospital stay was 13.6 days (7–23), showing geographic variability (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 microscopically 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 pancreaticoduodenectomy (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 systemÒ (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,
123
Surg Endosc
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 specific complications of minimally invasive approaches.
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
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 systemÒ 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 procedure,’’ or ‘‘pancreatic resection.’’ The final search was completed by June 1, 2013. Relevant articles identified by cross-referencing were also retrieved and reviewed. Articles 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 gastroduodenal 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/duodenal jejunal loop, conversion rate, operative time, blood loss, length of hospital stay, overall morbidity, overall
123
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 published 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 frequency (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 dissect the posterior margin and to perform digestive reconstruction (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 %), infraumbilical 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
Fig. 1 Flowchart of systematic review
Fig. 2 Number of studies published yearly
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 provided 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 electrocautery 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;
Fig. 3 Number of laparoscopic pancreaticoduodenectomies by country
Fig. 4 Number of laparoscopic pancreaticoduodenectomies by surgical technique
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
123
Surg Endosc Table 1 Articles reporting pancreaticoduodenectomies
on
five
or
Publication year
more
laparoscopic
First author [Ref.]
Country
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
Zhan [26]
China
2013
RA
Asbun [9]
US
2012
PL
42
Chalikonda [27]
US
2012
RA
30
Kuroki [20]
Japan
2012
LA
20
Lai [28] Nakamura [21]
China Japan
2012 2012
RA LA
20 12
100 16
Suzuki [22]
Japan
2012
LA
6
Zeh [31]
US
2012
RA
50
Zhou [29]
China
2011
RA
8
Ammori [17]
UK
2011
PL, HA
Zureikat [10]
US
2011
PL
14
7
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 pancreaticoduodenectomy, RA robotic-assisted pancreaticoduodenectomy, UK United Kingdom, US United States
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).
123
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 articles, 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 frequently. 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 measures is presented in Table 5.
5
7
5
Palanivelu [12]
Gumbs [13]
5
Zhou [29]
6
7
Zeh [31]
Cho [23]
5
Suzuki [22]
Narula [32]
6
6–7
5
Lai [28]
Nakamura [21]
Kendrick [11]
NA
6
Kuroki [20]
5
6
Chalikonda [27]
6 5
Right paraumbilical
5 6
Zhan [26] Asbun [9]
Ammori [17]
Infra-umbilical
5
Kim [16]
Zureikat [10] Giulianotti [30]
Umbilical
5
Corcione [8]
Umbilical
Right paraumbilical
Umbilical
Umbilical
NA
NA
Umbilical Right pararectal
Right paraumbilical
Umbilical
Umbilical
NA
Umbilical NA
Right pararectal
Supraumbilical
Infra-umbilical
5–6
4
Right pararectal
Lei [19]
5
Boggi [25]
Optic port
Lee [24]
No. of ports
First author [Ref.]
–
–
–
NA
NA
– Right
–
Right
Right
–
–
Left
–
NA
Right –
–
–
Left
Fourth robotic arm
Bipolar and Ultrasonic shears
Ultrasonic shears
Ultrasonic and radiofrequency shears
Ultrasonic shears
Ultrasonic shears
NA Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Radiofrequency shears
Ultrasonic and radiofrequency shears
NA
Radiofrequency shears
Ultrasonic shears
Ultrasonic and radiofrequency shears
Ultrasonic shears NA
Ultrasonic shears
Ultrasonic and radiofrequency shears
Ultrasonic and radiofrequency shears
Radiofrequency shears
Ultrasonic shears
Energy device
Table 2 Technical details of laparoscopic pancreaticoduodenectomy
Clips and suture ligature
NA
Clips
Ligature and clips
Clips
Vascular stapler Ligature
NA
NA
Ligature plus vascular stapler or suture ligature
Ligature
NA
Clips
NA
Clips
NA NA
Clips
NA
Radiofrequency shears
NA
Ligature
Closure of GDA
Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Electrocautery or Ultrasonic shears
NA Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Electrocautery
Radiofrequency shears
Stapler
Electrocautery
Ultrasonic shears
Ultrasonic shears
NA Ultrasonic shears
Stapler or Ultrasonic shears
NA
Ultrasonic shears
NA
Electrocautery
Section of pancreatic neck
Subxiphoid
Umbilical
Umbilical
Supra-umbilical
Infra-umbilical
Right lower quadrant Suprapubic
Variable
Infra-umbilical or suprapubic
Right lower quadrant
Supra-umbilical
Subxiphoid
Suprapubic
Subxiphoid
Umbilical
Enlarged torcar site Umbilical
Umbilical
Supra-umbilical
Subxiphoid
Suprapubic
Extraction site
NA
Yes
NA
Yes
No
Yes Yes
Yes
NA
Yes
NA
NA
Yes
NA
Yes
Yes Yes
Yes
NA
Yes
Yes
Yes
Drains
Surg Endosc
123
Yes
Yes NA
Umbilical Ultrasonic shears
Ultrasonic shears
Radiofrequency shears
Electrocautery or Ultrasonic shears
–
–
Clips
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 hospital 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 postoperative 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].
Clips or stapler
Yes Umbilical Ultrasonic shears Ultrasonic and radiofrequency shears –
Clips
Energy device Fourth robotic arm
Closure of GDA
Section of pancreatic neck
Extraction site
Drains
Surg Endosc
123
NA not available
6 Gagner [18]
NA
5 Dulucq [15]
Umbilical
4 Pugliese [14]
Umbilical
No. of ports First author [Ref.]
Table 2 continued
Optic port
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 pancreatic
Surg Endosc Table 3 Management of pancreatic stump in laparoscopic pancreaticoduodenectomy
First author [Ref.]
Boggi [25]
Duct management technique
Stent
PJ
PG
DO
34 (100 %)
0
0
NA
Suture Technique RS
DL
No
Yes
[D-to-M or E-to-S] Lee [24]
0
42 (100 %)
0
NA
NA
NA
Lei [19]
11 (100 %)
0
0
Yes (10/11)
No
Yes
13 (59 %)
3 (13.6 %)
6 (27.2 %)
NA
NA
NA
0
0
NA
NA
Yes
Corcione [8]
[10 E-to-E; 3 D-to-M] Kim [16]
90 (100 %) [E-to-E normal PD; D-to-M enlarged PD]
Zhan [26]
NA
NA
NA
NA
NA
NA
Asbun [9]
42 (100 %)
0
0
Yes
No
Yes
0
0
Yes
No
Yes
0
0
NA
NA
Yes
0
0
Selectively
NA
Yes
0
0
Yes
No
Yes
3 (50 %)
0
Yes
No
Yes
[D-to-M] Chalikonda [27]
30 (100 %) [D-to-M]
Kuroki [20]
20 (100 %) [D-to-M]
Lai [28]
20 (100 %) [D-to-M (PD [ 3 mm).
Nakamura [21]
Dunking (PD B 3 mm)] 12 (100 %) [Kakita’s technique]
Suzuki [22]
3 (50 %) [D-to-M]
Zeh [31]
50 (100 %)
[In PJ] 0
0
Yes
No
Yes
0
0
NA
NA
Yes
0
0
Yes
*
No
0
0
NA
Yes
Yes
[D-to-M] Zhou [29]
8 (100 %) [E-to-S]
Ammori [17]
7 (100 %) [E-to-S or D-to-M]
Zureikat [10]
14 (100 %) [D-to-M]
Giulianotti [30]
0
19 (31.6 %)
41 (68.3 %)
NA
Yes
NA
Kendrick [11]
62 (100 %)
0
0
Yes
No
Yes
[D-to-M]
DL double layer, DO duct occlusion, D-t-M duct-tomucosa, E-to-E end-to-end, Eto-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
Narula [32]
8 (100 %) [D-to-M]
0
0
NA
No
Yes
Cho [23]
15 (100 %)
0
0
NA
NA
NA
0
0
No
No
Yes
[E-to-S] Palanivelu [12]
75 (100 %) [E-to-S]
Gumbs [13]
NA
NA
NA
NA
NA
NA
Pugliese [14]
19 (100 %)
0
0
Yes
Yes
No
[E-to-S] Dulucq [15]
25 (100 %)
0
0
No
Yes
No
Gagner [18]
10 (100 %)
0
0
Yes
No
Yes
123
Surg Endosc Table 4 Management of gastric/duodenal stump in laparoscopic pancreaticoduodenectomy First author [Ref.]
Antrectomy Yes
Loop route No
Anastomotic technique
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] Chalikonda [27]
3 (7.1 %) 0
39 (92.8 %) 30 (100 %)
0 0
0 0
42 (100 %) 30 (100 %)
39 (92.8 %) 30 (100 %)
3 (7.1 %) 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] Pugliese [14]
NA 14 (73.6 %)
NA 5 (26.3 %)
NA 0
NA 19 (100 %)
NA 0
NA 5 (26.3 %)
NA 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
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
123
adenocarcinoma. Overall, there were 194 pancreatic ductal adenocarcinomas (30.6 %), 327 other malignant or borderline 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
Surg Endosc 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 5.6 %
Asbun* [9]
16.9 %
541 ± 88
195 ± 136
8 ± 3.2
47.1 %
16.7 %
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] Suzuki [22]
NA 16.6 %
NA 581 (507–817)
NA 475 (415–3,860)
NA 23 (11–36)
NA 33.3 %
NA 33.3 %
0 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 % 3.3 %
Giulianotti [30]
18.3 %
421 (240–660)
394 (80–1,500)
22 (5–85)
NA
31.6 %
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 postoperative 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
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
123
Surg Endosc Table 7 Comparison of surgical techniques for LPD
PL (n = 188) WA of operative time (min) WA of EBL (mL) Pancreatic fistula (n, %) Morbidity (n, %) Mortality (n, %)
* t test unpaired, ^ Fisher exact test
1 (1.1 %)
5 (2.4 %)
(n = 188)
(n = 95)
(n = 210)
0.0092^
(n = 533) 274.22
(n = 533) 386.29
0.0001^
(n = 433)
(n = 142)
3 (1.6 %) (n = 187)
NS° NS° NS° NS°
* Chi squared, ^ t test unpaired, ° Fisher exact test
[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 adaptation to limited resource availability. Perhaps the latter issue is one of the reasons accounting for the patchy geographical 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 followed 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
123
NS^
5 (2.7 %)
69 (32.3 %)
11 (2.0 %)
NS^
(n = 218)
467.42
(n = 533)
NS^
94 (43.1 %)
(n = 63)
447.73
Mortality (%)
NS^
21 (33.3 %)
(n = 153)
52 (9.7 %)
40 (21.8 %)
NS^
61 (39.9 %)
LA
(n = 183)
NS^
(n = 218)
52 (24.4 %)
117 (23.4 %)
0.005^
55 (25.2 %)
5 (2.3 %)
(n = 498)
0.02^
35 (42.2 %) (n = 83)
0
Pancreatic fistula (%)
0.0001^
23 (15.0 %)
182 (34.1 %)
69 (39.8 %)
0.02*
(n = 153)
HA
(n = 173)
0.0001*
346.6 (n = 218)
RA
183 (41.7 %)
0.0001*
395.0 (n = 83)
0.0005*
(n = 438)
0.0004*
171.3
87 (40.8 %)
Morbidity (%)
0.0001*
(n = 166)
299 (56.0 %)
22 (10.9 %)
0.0001*
508.2
PL
(n = 142)
LA vs RA
(n = 226)
Technique (n, %)
(n = 498)
PL vs RA
465.9
p
40 (8.0 %)
PL vs LA
(n = 83)
Smaller series (n = 213)
Conversion (%)
p
(n = 188)
Large series (n = 533)
WA of blood loss (mL)
RA (n = 226)
410.1
Table 8 Comparison of large vs smaller series
WA of operative time (min.)
LA (n = 95)
the pancreatic head makes it necessary to place the handassisted 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 reconstructions. 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 operative 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 conveniently 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 laparoscopists, that costs of RA laparoscopy remain high [25], and that the da Vinci Surgical SystemÒ 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], intricacy of instrument exchange disrupting the flow of the
Surg Endosc Table 9 Main pathology parameters in laparoscopic pancreaticoduodenectomy
First author [Ref.]
Tumor type PDAC
Lymph nodes Potentially malignant tumors
R0
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] Chalikonda [27]
NA 14 (46.6 %)
NA 4 (13.3 %)
NA 12 (40.0 %)
23.44 ± 10.1 13.2 (1–37)
94.9 % 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
89.1 %
14 (12–45) USA
NA not available
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] Gumbs [13]
23 (30.6 %) NA
49 (65.3 %) NA
3 (4.0 %) NA
14 (8–22) NA
97.2 % 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
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 limitations, everyone who has had the opportunity to test the da Vinci Surgical SystemÒ recognizes that it enhances surgeon 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 Trendelenburg’s position. The use of ultrasonic shears is prevalent among energy devices, while clips and/or ligature are preferred to seal the gastroduodenal artery. The specimen is often extracted through an umbilical or periumbilical incision, and drains are left near the pancreatic anastomosis. When RA laparoscopy is employed, the socalled ‘‘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
123
Surg Endosc
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-established 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 duodenum 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 mesentericportal vein is a major issue in LPD, including RA laparoscopy. 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 occurred 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 laparoscopic operations, such as colectomy, shows that prolonged operative time entails increased postoperative
123
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 dissection 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 operating room time and allows patients with reduced physiologic 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 complications, it reasonable to assume that cultural and organizational issues account at least for some of these differences [30]. Unfortunately, information on readmission 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 standardized criteria. In particular, regarding pancreatic fistula, it should be considered that a relevant proportion of patients undergoing LPD were operated on because of periampullary 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 reasonably 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
31] further suggesting that LPD is equivalent to open PD as a cancer operation, in properly selected patients. Confirmation 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 outcome 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 convincing answers until specifically designed prospective studies, including randomized comparisons with the open operation, 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.
References 1. Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410 2. Subhas G, Mittal VK (2011) Training minimal invasive approaches in hepatopancreatobilliary fellowship: the current status. HPB (Oxford) 13:149–152 3. Boggi U, Signori S, Vistoli F, D’Imporzano S, Amorese G, Consani G, Guarracino F, Marchetti P, Focosi D, Mosca F (2012) Laparoscopic robot-assisted pancreas transplantation: first world experience. Transplantation 93:201–206 4. Boggi U, Vistoli F, Signori S, D’Imporzano S, Amorese G, Consani G, Guarracino F, Melfi F, Mussi A, Mosca F (2011) Robotic renal transplantation: first European case. Transpl Int 24:213–218 5. Lin NC, Nitta H, Wakabayashi G (2013) Laparoscopic major hepatectomy: a systematic literature review and comparison of 3 techniques. Ann Surg 257:205–213 6. Kim VB, Chapman WH, Albrecht RJ, Bailey BM, Young JA, Nifong LW, Chitwood WR Jr (2002) Early experience with telemanipulative robot-assisted laparoscopic cholecystectomy using da Vinci. Surg Laparosc Endosc Percutan Tech 12:33–40 7. Fingerhut A (2011) Surgical ego, the good, the bad, and the ugly. Surg Innov 18:97–98 8. Corcione F, Pirozzi F, Cuccurullo D, Piccolboni D, Caracino V, Galante F, Cusano D, Sciuto A (2013) Laparoscopic pancreaticoduodenectomy: experience of 22 cases. Surg Endosc 27:2131–2316 9. Asbun HJ, Stauffer JA (2012) Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the accordion severity grading system. J Am Coll Surg 215:810–819
10. Zureikat AH, Breaux JA, Steel JL, Hughes SJ (2011) Can laparoscopic pancreaticoduodenectomy be safely implemented? J Gastrointest Surg 15:1151–1157 11. Kendrick ML, Cusati D (2010) Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch Surg 145:19–23 12. Palanivelu C, Rajan PS, Rangarajan M, Vaithiswaran V, Senthilnathan P, Parthasarathi R, Praveen Raj P (2009) Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary Pancreat Surg 16:731–740 13. Gumbs AA, Gayet B (2008) The laparoscopic duodenopancreatectomy: the posterior approach. Surg Endosc 22:539–540 14. Pugliese R, Scandroglio I, Sansonna F, Maggioni D, Costanzi A, Citterio D, Ferrari GC, Di Lernia S, Magistro C (2008) Laparoscopic pancreaticoduodenectomy: a retrospective review of 19 cases. Surg Laparosc Endosc Percutan Tech 18:13–18 15. Dulucq JL, Wintringer P, Mahajna A (2006) Laparoscopic pancreaticoduodenectomy for benign and malignant diseases. Surg Endosc 20:1045–1050 16. Kim SC, Song KB, Jung YS, Kim YH, Park do H, Lee SS, Seo DW, Lee SK, Kim MH, Park KM, Lee YJ (2013) Short-term clinical outcomes for 100 consecutive cases of laparoscopic pylorus-preserving pancreatoduodenectomy: improvement with surgical experience. Surg Endosc 27:95–103 17. Ammori BJ, Ayiomamitis GD (2011) Laparoscopic pancreaticoduodenectomy and distal pancreatectomy: a UK experience and a systematic review of the literature. Surg Endosc 25:2084–2099 18. Gagner M, Pomp A (1997) Laparoscopic pancreatic resection: is it worthwhile? J Gastrointest Surg 1:20–25 19. Lei Z, Zhifei W, Jun X, Chang L, Lishan X, Yinghui G, Bo Z (2013) Pancreaticojejunostomy sleeve reconstruction after pancreaticoduodenectomy in laparoscopic and open surgery. JSLS 17:68–73 20. Kuroki T, Adachi T, Okamoto T, Kanematsu T (2012) A nonrandomized comparative study of laparoscopy-assisted pancreaticoduodenectomy and open pancreaticoduodenectomy. Hepatogastroenterology 59:570–573 21. Nakamura Y, Matsumoto S, Matsushita A, Yoshioka M, Shimizu T, Yamahatsu K, Uchida E (2012) Pancreaticojejunostomy with closure of the pancreatic stump by endoscopic linear stapler in laparoscopic pancreaticoduodenectomy: a reliable technique and benefits for pancreatic resection. Asian J Endosc Surg 5:191–194 22. Suzuki O, Kondo S, Hirano S, Tanaka E, Kato K, Tsuchikawa T, Yano T, Okamura K, Shichinohe T (2012) Laparoscopic pancreaticoduodenectomy combined with minilaparotomy. Surg Today 42:509–513 23. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, Souda H, Gunji H, Miyazaki A, Ikeda A, Tohma T, Matsumoto I (2009) Comparison of laparoscopy-assisted and open pylorus-preserving pancreaticoduodenectomy for periampullary disease. Am J Surg 198:445–449 24. Lee JS, Han JH, Na GH, Choi HJ, Hong TH, You YK, Kim DG (2013) Laparoscopic pancreaticoduodenectomy assisted by minilaparotomy. Surg Laparosc Endosc Percutan Tech 23:e98–e102 25. Boggi U, Signori S, De Lio N, Perrone VG, Vistoli F, Belluomini M, Cappelli C, Amorese G, Mosca F (2013) Feasibility of robotic pancreaticoduodenectomy. Br J Surg 100:917–925 26. Zhan Q, Deng XX, Han B, Liu Q, Shen BY, Peng CH, Li HW (2013) Robotic-assisted pancreatic resection: a report of 47 cases. Int J Med Robot 9:44–51 27. Chalikonda S, Aguilar-Saavedra JR, Walsh RM (2012) Laparoscopic robotic-assisted pancreaticoduodenectomy: a case-matched comparison with open resection. Surg Endosc 26:2397–2402
123
Surg Endosc 28. Lai EC, Yang GP, Tang CN (2012) Robot-assisted laparoscopic pancreaticoduodenectomy versus open pancreaticoduodenectomy—a comparative study. Int J Surg 10:475–479 29. Zhou NX, Chen JZ, Liu Q, Zhang X, Wang Z, Ren S, Chen XF (2011) Outcomes of pancreatoduodenectomy with robotic surgery versus open surgery. Int J Med Robot 7:131–137 30. Giulianotti PC, Sbrana F, Bianco FM, Elli EF, Shah G, Addeo P, Caravaglios G, Coratti A (2010) Robot-assisted laparoscopic pancreatic surgery: single-surgeon experience. Surg Endosc 24:1646–1657 31. Zeh HJ, Zureikat AH, Secrest A, Dauoudi M, Bartlett D, Moser AJ (2012) Outcomes after robot-assisted pancreaticoduodenectomy for periampullary lesions. Ann Surg Oncol 19:864–870 32. Narula VK, Mikami DJ, Melvin WS (2010) Robotic and laparoscopic pancreaticoduodenectomy: a hybrid approach. Pancreas 39:160–164 33. Gumbs AA, Rodriguez Rivera AM, Milone L, Hoffman JP (2011) Laparoscopic pancreatoduodenectomy: a review of 285 published cases. Ann Surg Oncol 18:1335–1341 34. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M; International Study Group on Pancreatic Fistula Definition (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13 35. Horiguchi A, Uyama I, Miyakawa S (2011) Robot-assisted laparoscopic pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci 18:287–291 36. Choi SH, Kang CM, Kim DH, Lee WJ, Chi HS (2011) Robotic pylorus preserving pancreaticoduodenectomy with mini-laparotomy reconstruction in a patient with ampullary adenoma. J Korean Surg Soc 81:355–359 37. Machado MA, Makdissi FF, Surjan RC, Machado MC (2013) Laparoscopic pylorus-preserving pancreatoduodenectomy with double jejunal loop reconstruction: an old trick for a new dog. J Laparoendosc Adv Surg Tech A 23:146–149 38. Kimura Y, Hirata K, Mukaiya M, Mizuguchi T, Koito K, Katsuramaki T (2005) Hand-assisted laparoscopic pylorus preserving pancreaticoduodenectomy for pancreas head disease. Am J Surg 189:734–737 39. Keck T, Kuesters S, Wellner U, Hopt UT, Karcz WK (2011) Laparoscopic pylorus-preserving pancreatic head resection and hybrid open reconstruction via pancreatogastrostomy. J Gastrointest Surg 15:373–377 40. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, Souda H, Gunji H, Miyazaki A, Ikeda A, Tohma T (2009) A totally laparoscopic pylorus preserving pancreaticoduodenectomy and reconstruction. Surg Today 39:359–362 41. Matsuoka L, Parekh D (2012) The minimally invasive approach to surgical management of pancreatic diseases. Gastroenterol Clin North Am 41:77–101 42. Fisher WE, Hodges SE, Wu MF, Hilsenbeck SG, Brunicardi FC (2012) Assessment of the learning curve for pancreaticoduodenectomy. Am J Surg 203:684–690 43. Vaessen C (2011) Location of robotic surgical systems worldwide and in France. J Visc Surg 148:e9–e11 44. Cuschieri A (2000) Laparoscopic hand-assisted surgery for hepatic and pancreatic disease. Surg Endosc 14:991–996 45. Velidedeoglu E, Williams N, Brayman KL, Desai NM, Campos L, Palanjian M, Wocjik M, Bloom R, Grossman RA, Mange K, Barker CF, Naji A, Markmann JF (2002) Comparison of open, laparoscopic, and hand-assisted approaches to live-donor nephrectomy. Transplantation 74:169–172 46. Kaban GK, Czerniach DR, Cohen R, Novitsky YW, Yood SM, Perugini RA, Kelly JJ, Litwin DE (2004) Hand-assisted laparoscopic splenectomy in the setting of splenomegaly. Surg Endosc 18:1340–1343
123
47. Moorthy K, Munz Y, Dosis A, Hernandez J, Martin S, Bello F, Rockall T, Darzi A (2004) Dexterity enhancement with robotic surgery. Surg Endosc 18:790–795 48. Mucksavage P, Kerbl DC, Lee JY (2011) The da VinciÒ surgical system overcomes innate hand dominance. J Endourol 25:1385–1388 49. Maniar HS, Council ML, Prasad SM, Prasad SM, Chu C, Damiano RJ Jr (2005) Comparison of skill training with robotic systems and traditional endoscopy: implications on training and adoption. J Surg Res 125:23–29 50. Heemskerk J, van Gemert WG, de Vries J, Greve J, Bouvy ND (2007) Learning curves of robot-assisted laparoscopic surgery compared with conventional laparoscopic surgery: an experimental study evaluating skill acquisition of robot-assisted laparoscopic tasks compared with conventional laparoscopic tasks in inexperienced users. Surg Laparosc Endosc Percutan Tech 17:171–174 51. Zeh HJ 3rd, Bartlett DL, Moser AJ (2011) Robotic-assisted major pancreatic resection. Adv Surg 45:323–340 52. Sgarbura O, Vasilescu C (2010) The decisive role of the patientside surgeon in robotic surgery. Surg Endosc 24:3149–3155 53. Boggi U, Moretto C, Vistoli F, D’Imporzano S, Mosca F (2009) Robotic suture of a large caval injury caused by endo-GIA stapler malfunction during laparoscopic wedge resection of liver segments VII and VIII en-bloc with the right hepatic vein. Minim Invasive Ther Allied Technol 18:306–310 54. Lee HC, Yun MJ, Goo EK, Bahk JH, Park HP, Jeon YT, Lee SC (2010) Rupture of endotracheal tube cuff during robot-assisted endoscopic thyroidectomy—a case report. Korean J Anesthesiol 59:416–419 55. Strasberg SM, Drebin JA, Mokadam NA, Green DW, Jones KL, Ehlers JP, Linehan D (2002) Prospective trial of a blood supplybased technique of pancreaticojejunostomy: effect on anastomotic failure in the Whipple procedure. J Am Coll Surg 194:746–758 56. La¨msa¨ T, Jin HT, Nordback PH, Sand J, Luukkaala T, Nordback I (2009) Pancreatic injury response is different depending on the method of resecting the parenchyma. J Surg Res 154:203–211 57. Emam TA, Cuschieri A (2003) How safe is high-power ultrasonic dissection? Ann Surg 237:186–191 58. Druzˇijanic´ N, Pogorelic´ Z, Perko Z, Mrklic´ I, Tomic´ S (2012) Comparison of lateral thermal damage of the human peritoneum using monopolar diathermy, Harmonic scalpel and LigaSure. Can J Surg 55:317–321 59. Boggi U, Caniglia F, Amorese G (2014) Laparoscopic robotassisted major hepatectomy. J Hepatobiliary Pancreat Sci 21:3–10 60. Owen RM, Perez SD, Lytle N, Patel A, Davis SS, Lin E, Sweeney JF (2013) Impact of operative duration on postoperative pulmonary complications in laparoscopic versus open colectomy. Surg Endosc 27:3555–3563 61. Evans C, Lim J, Gatzen C, Huang A (2012) Factors influencing laparoscopic colorectal operative duration and its effect on clinical outcome. Surg Laparosc Endosc Percutan Tech 22:437–442 62. Procter LD, Davenport DL, Bernard AC, Zwischenberger JB (2010) General surgical operative duration is associated with increased risk-adjusted infectious complication rates and length of hospital stay. J Am Coll Surg 210:60–65 63. Cameron JL, Riall TS, Coleman J, Belcher KA (2006) One thousand consecutive pancreaticoduodenectomies. Ann Surg 244:10–15 64. Bernard AC, Davenport DL, Chang PK, Vaughan TB, Zwischenberger JB (2009) Intraoperative transfusion of 1 U to 2 U packed red blood cells is associated with increased 30-day mortality, surgical-site infection, pneumonia, and sepsis in general surgery patients. J Am Coll Surg 208:931–937
Surg Endosc 65. Zhang J, Wu WM, You L, Zhao YP (2013) Robotic versus open pancreatectomy: a systematic review and meta-analysis. Ann Surg Oncol 20:1774–1780 66. Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM Jr (2013) A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg 216:1–14 67. Verbeke CS, Leitch D, Menon KV, McMahon MJ, Guillou PJ, Anthoney A (2006) Redefining the R1 resection in pancreatic cancer. Br J Surg 93:1232–1237
68. Esposito I, Kleeff J, Bergmann F, Reiser C, Herpel E, Friess H, Schirmacher P, Bu¨chler MW (2008) Most pancreatic cancer resections are R1 resections. Ann Surg Oncol 15:1651–1660 69. Chun YS, Milestone BN, Watson JC, Cohen SJ, Burtness B, Engstrom PF, Haluszka O, Tokar JL, Hall MJ, Denlinger CS, Astsaturov I, Hoffman JP (2010) Defining venous involvement in borderline resectable pancreatic cancer. Ann Surg Oncol 17:2832–2838
123
and Other Interventional Techniques
REVIEW
Laparoscopic pancreaticoduodenectomy: a systematic literature 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 Ó 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 appropriateness. 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 %), laparoscopic assistance (LA) in 121 (16.2 %), and hand assistance 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
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: [email protected] G. Amorese Division of General and Vascular Anesthesia and Intensive Care, Pisa University Hospital, Pisa, Italy
in 22.3 % of patients (4.5–52.3 %). Mean length of hospital stay was 13.6 days (7–23), showing geographic variability (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 microscopically 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 pancreaticoduodenectomy (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 systemÒ (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,
123
Surg Endosc
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 specific complications of minimally invasive approaches.
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
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 systemÒ 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 procedure,’’ or ‘‘pancreatic resection.’’ The final search was completed by June 1, 2013. Relevant articles identified by cross-referencing were also retrieved and reviewed. Articles 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 gastroduodenal 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/duodenal jejunal loop, conversion rate, operative time, blood loss, length of hospital stay, overall morbidity, overall
123
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 published 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 frequency (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 dissect the posterior margin and to perform digestive reconstruction (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 %), infraumbilical 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
Fig. 1 Flowchart of systematic review
Fig. 2 Number of studies published yearly
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 provided 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 electrocautery 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;
Fig. 3 Number of laparoscopic pancreaticoduodenectomies by country
Fig. 4 Number of laparoscopic pancreaticoduodenectomies by surgical technique
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
123
Surg Endosc Table 1 Articles reporting pancreaticoduodenectomies
on
five
or
Publication year
more
laparoscopic
First author [Ref.]
Country
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
Zhan [26]
China
2013
RA
Asbun [9]
US
2012
PL
42
Chalikonda [27]
US
2012
RA
30
Kuroki [20]
Japan
2012
LA
20
Lai [28] Nakamura [21]
China Japan
2012 2012
RA LA
20 12
100 16
Suzuki [22]
Japan
2012
LA
6
Zeh [31]
US
2012
RA
50
Zhou [29]
China
2011
RA
8
Ammori [17]
UK
2011
PL, HA
Zureikat [10]
US
2011
PL
14
7
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 pancreaticoduodenectomy, RA robotic-assisted pancreaticoduodenectomy, UK United Kingdom, US United States
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).
123
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 articles, 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 frequently. 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 measures is presented in Table 5.
5
7
5
Palanivelu [12]
Gumbs [13]
5
Zhou [29]
6
7
Zeh [31]
Cho [23]
5
Suzuki [22]
Narula [32]
6
6–7
5
Lai [28]
Nakamura [21]
Kendrick [11]
NA
6
Kuroki [20]
5
6
Chalikonda [27]
6 5
Right paraumbilical
5 6
Zhan [26] Asbun [9]
Ammori [17]
Infra-umbilical
5
Kim [16]
Zureikat [10] Giulianotti [30]
Umbilical
5
Corcione [8]
Umbilical
Right paraumbilical
Umbilical
Umbilical
NA
NA
Umbilical Right pararectal
Right paraumbilical
Umbilical
Umbilical
NA
Umbilical NA
Right pararectal
Supraumbilical
Infra-umbilical
5–6
4
Right pararectal
Lei [19]
5
Boggi [25]
Optic port
Lee [24]
No. of ports
First author [Ref.]
–
–
–
NA
NA
– Right
–
Right
Right
–
–
Left
–
NA
Right –
–
–
Left
Fourth robotic arm
Bipolar and Ultrasonic shears
Ultrasonic shears
Ultrasonic and radiofrequency shears
Ultrasonic shears
Ultrasonic shears
NA Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Radiofrequency shears
Ultrasonic and radiofrequency shears
NA
Radiofrequency shears
Ultrasonic shears
Ultrasonic and radiofrequency shears
Ultrasonic shears NA
Ultrasonic shears
Ultrasonic and radiofrequency shears
Ultrasonic and radiofrequency shears
Radiofrequency shears
Ultrasonic shears
Energy device
Table 2 Technical details of laparoscopic pancreaticoduodenectomy
Clips and suture ligature
NA
Clips
Ligature and clips
Clips
Vascular stapler Ligature
NA
NA
Ligature plus vascular stapler or suture ligature
Ligature
NA
Clips
NA
Clips
NA NA
Clips
NA
Radiofrequency shears
NA
Ligature
Closure of GDA
Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Electrocautery or Ultrasonic shears
NA Ultrasonic shears
Ultrasonic shears
Ultrasonic shears
Electrocautery
Radiofrequency shears
Stapler
Electrocautery
Ultrasonic shears
Ultrasonic shears
NA Ultrasonic shears
Stapler or Ultrasonic shears
NA
Ultrasonic shears
NA
Electrocautery
Section of pancreatic neck
Subxiphoid
Umbilical
Umbilical
Supra-umbilical
Infra-umbilical
Right lower quadrant Suprapubic
Variable
Infra-umbilical or suprapubic
Right lower quadrant
Supra-umbilical
Subxiphoid
Suprapubic
Subxiphoid
Umbilical
Enlarged torcar site Umbilical
Umbilical
Supra-umbilical
Subxiphoid
Suprapubic
Extraction site
NA
Yes
NA
Yes
No
Yes Yes
Yes
NA
Yes
NA
NA
Yes
NA
Yes
Yes Yes
Yes
NA
Yes
Yes
Yes
Drains
Surg Endosc
123
Yes
Yes NA
Umbilical Ultrasonic shears
Ultrasonic shears
Radiofrequency shears
Electrocautery or Ultrasonic shears
–
–
Clips
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 hospital 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 postoperative 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].
Clips or stapler
Yes Umbilical Ultrasonic shears Ultrasonic and radiofrequency shears –
Clips
Energy device Fourth robotic arm
Closure of GDA
Section of pancreatic neck
Extraction site
Drains
Surg Endosc
123
NA not available
6 Gagner [18]
NA
5 Dulucq [15]
Umbilical
4 Pugliese [14]
Umbilical
No. of ports First author [Ref.]
Table 2 continued
Optic port
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 pancreatic
Surg Endosc Table 3 Management of pancreatic stump in laparoscopic pancreaticoduodenectomy
First author [Ref.]
Boggi [25]
Duct management technique
Stent
PJ
PG
DO
34 (100 %)
0
0
NA
Suture Technique RS
DL
No
Yes
[D-to-M or E-to-S] Lee [24]
0
42 (100 %)
0
NA
NA
NA
Lei [19]
11 (100 %)
0
0
Yes (10/11)
No
Yes
13 (59 %)
3 (13.6 %)
6 (27.2 %)
NA
NA
NA
0
0
NA
NA
Yes
Corcione [8]
[10 E-to-E; 3 D-to-M] Kim [16]
90 (100 %) [E-to-E normal PD; D-to-M enlarged PD]
Zhan [26]
NA
NA
NA
NA
NA
NA
Asbun [9]
42 (100 %)
0
0
Yes
No
Yes
0
0
Yes
No
Yes
0
0
NA
NA
Yes
0
0
Selectively
NA
Yes
0
0
Yes
No
Yes
3 (50 %)
0
Yes
No
Yes
[D-to-M] Chalikonda [27]
30 (100 %) [D-to-M]
Kuroki [20]
20 (100 %) [D-to-M]
Lai [28]
20 (100 %) [D-to-M (PD [ 3 mm).
Nakamura [21]
Dunking (PD B 3 mm)] 12 (100 %) [Kakita’s technique]
Suzuki [22]
3 (50 %) [D-to-M]
Zeh [31]
50 (100 %)
[In PJ] 0
0
Yes
No
Yes
0
0
NA
NA
Yes
0
0
Yes
*
No
0
0
NA
Yes
Yes
[D-to-M] Zhou [29]
8 (100 %) [E-to-S]
Ammori [17]
7 (100 %) [E-to-S or D-to-M]
Zureikat [10]
14 (100 %) [D-to-M]
Giulianotti [30]
0
19 (31.6 %)
41 (68.3 %)
NA
Yes
NA
Kendrick [11]
62 (100 %)
0
0
Yes
No
Yes
[D-to-M]
DL double layer, DO duct occlusion, D-t-M duct-tomucosa, E-to-E end-to-end, Eto-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
Narula [32]
8 (100 %) [D-to-M]
0
0
NA
No
Yes
Cho [23]
15 (100 %)
0
0
NA
NA
NA
0
0
No
No
Yes
[E-to-S] Palanivelu [12]
75 (100 %) [E-to-S]
Gumbs [13]
NA
NA
NA
NA
NA
NA
Pugliese [14]
19 (100 %)
0
0
Yes
Yes
No
[E-to-S] Dulucq [15]
25 (100 %)
0
0
No
Yes
No
Gagner [18]
10 (100 %)
0
0
Yes
No
Yes
123
Surg Endosc Table 4 Management of gastric/duodenal stump in laparoscopic pancreaticoduodenectomy First author [Ref.]
Antrectomy Yes
Loop route No
Anastomotic technique
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] Chalikonda [27]
3 (7.1 %) 0
39 (92.8 %) 30 (100 %)
0 0
0 0
42 (100 %) 30 (100 %)
39 (92.8 %) 30 (100 %)
3 (7.1 %) 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] Pugliese [14]
NA 14 (73.6 %)
NA 5 (26.3 %)
NA 0
NA 19 (100 %)
NA 0
NA 5 (26.3 %)
NA 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
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
123
adenocarcinoma. Overall, there were 194 pancreatic ductal adenocarcinomas (30.6 %), 327 other malignant or borderline 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
Surg Endosc 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 5.6 %
Asbun* [9]
16.9 %
541 ± 88
195 ± 136
8 ± 3.2
47.1 %
16.7 %
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] Suzuki [22]
NA 16.6 %
NA 581 (507–817)
NA 475 (415–3,860)
NA 23 (11–36)
NA 33.3 %
NA 33.3 %
0 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 % 3.3 %
Giulianotti [30]
18.3 %
421 (240–660)
394 (80–1,500)
22 (5–85)
NA
31.6 %
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 postoperative 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
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
123
Surg Endosc Table 7 Comparison of surgical techniques for LPD
PL (n = 188) WA of operative time (min) WA of EBL (mL) Pancreatic fistula (n, %) Morbidity (n, %) Mortality (n, %)
* t test unpaired, ^ Fisher exact test
1 (1.1 %)
5 (2.4 %)
(n = 188)
(n = 95)
(n = 210)
0.0092^
(n = 533) 274.22
(n = 533) 386.29
0.0001^
(n = 433)
(n = 142)
3 (1.6 %) (n = 187)
NS° NS° NS° NS°
* Chi squared, ^ t test unpaired, ° Fisher exact test
[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 adaptation to limited resource availability. Perhaps the latter issue is one of the reasons accounting for the patchy geographical 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 followed 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
123
NS^
5 (2.7 %)
69 (32.3 %)
11 (2.0 %)
NS^
(n = 218)
467.42
(n = 533)
NS^
94 (43.1 %)
(n = 63)
447.73
Mortality (%)
NS^
21 (33.3 %)
(n = 153)
52 (9.7 %)
40 (21.8 %)
NS^
61 (39.9 %)
LA
(n = 183)
NS^
(n = 218)
52 (24.4 %)
117 (23.4 %)
0.005^
55 (25.2 %)
5 (2.3 %)
(n = 498)
0.02^
35 (42.2 %) (n = 83)
0
Pancreatic fistula (%)
0.0001^
23 (15.0 %)
182 (34.1 %)
69 (39.8 %)
0.02*
(n = 153)
HA
(n = 173)
0.0001*
346.6 (n = 218)
RA
183 (41.7 %)
0.0001*
395.0 (n = 83)
0.0005*
(n = 438)
0.0004*
171.3
87 (40.8 %)
Morbidity (%)
0.0001*
(n = 166)
299 (56.0 %)
22 (10.9 %)
0.0001*
508.2
PL
(n = 142)
LA vs RA
(n = 226)
Technique (n, %)
(n = 498)
PL vs RA
465.9
p
40 (8.0 %)
PL vs LA
(n = 83)
Smaller series (n = 213)
Conversion (%)
p
(n = 188)
Large series (n = 533)
WA of blood loss (mL)
RA (n = 226)
410.1
Table 8 Comparison of large vs smaller series
WA of operative time (min.)
LA (n = 95)
the pancreatic head makes it necessary to place the handassisted 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 reconstructions. 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 operative 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 conveniently 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 laparoscopists, that costs of RA laparoscopy remain high [25], and that the da Vinci Surgical SystemÒ 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], intricacy of instrument exchange disrupting the flow of the
Surg Endosc Table 9 Main pathology parameters in laparoscopic pancreaticoduodenectomy
First author [Ref.]
Tumor type PDAC
Lymph nodes Potentially malignant tumors
R0
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] Chalikonda [27]
NA 14 (46.6 %)
NA 4 (13.3 %)
NA 12 (40.0 %)
23.44 ± 10.1 13.2 (1–37)
94.9 % 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
89.1 %
14 (12–45) USA
NA not available
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] Gumbs [13]
23 (30.6 %) NA
49 (65.3 %) NA
3 (4.0 %) NA
14 (8–22) NA
97.2 % 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
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 limitations, everyone who has had the opportunity to test the da Vinci Surgical SystemÒ recognizes that it enhances surgeon 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 Trendelenburg’s position. The use of ultrasonic shears is prevalent among energy devices, while clips and/or ligature are preferred to seal the gastroduodenal artery. The specimen is often extracted through an umbilical or periumbilical incision, and drains are left near the pancreatic anastomosis. When RA laparoscopy is employed, the socalled ‘‘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
123
Surg Endosc
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-established 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 duodenum 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 mesentericportal vein is a major issue in LPD, including RA laparoscopy. 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 occurred 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 laparoscopic operations, such as colectomy, shows that prolonged operative time entails increased postoperative
123
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 dissection 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 operating room time and allows patients with reduced physiologic 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 complications, it reasonable to assume that cultural and organizational issues account at least for some of these differences [30]. Unfortunately, information on readmission 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 standardized criteria. In particular, regarding pancreatic fistula, it should be considered that a relevant proportion of patients undergoing LPD were operated on because of periampullary 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 reasonably 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
31] further suggesting that LPD is equivalent to open PD as a cancer operation, in properly selected patients. Confirmation 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 outcome 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 convincing answers until specifically designed prospective studies, including randomized comparisons with the open operation, 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.
References 1. Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410 2. Subhas G, Mittal VK (2011) Training minimal invasive approaches in hepatopancreatobilliary fellowship: the current status. HPB (Oxford) 13:149–152 3. Boggi U, Signori S, Vistoli F, D’Imporzano S, Amorese G, Consani G, Guarracino F, Marchetti P, Focosi D, Mosca F (2012) Laparoscopic robot-assisted pancreas transplantation: first world experience. Transplantation 93:201–206 4. Boggi U, Vistoli F, Signori S, D’Imporzano S, Amorese G, Consani G, Guarracino F, Melfi F, Mussi A, Mosca F (2011) Robotic renal transplantation: first European case. Transpl Int 24:213–218 5. Lin NC, Nitta H, Wakabayashi G (2013) Laparoscopic major hepatectomy: a systematic literature review and comparison of 3 techniques. Ann Surg 257:205–213 6. Kim VB, Chapman WH, Albrecht RJ, Bailey BM, Young JA, Nifong LW, Chitwood WR Jr (2002) Early experience with telemanipulative robot-assisted laparoscopic cholecystectomy using da Vinci. Surg Laparosc Endosc Percutan Tech 12:33–40 7. Fingerhut A (2011) Surgical ego, the good, the bad, and the ugly. Surg Innov 18:97–98 8. Corcione F, Pirozzi F, Cuccurullo D, Piccolboni D, Caracino V, Galante F, Cusano D, Sciuto A (2013) Laparoscopic pancreaticoduodenectomy: experience of 22 cases. Surg Endosc 27:2131–2316 9. Asbun HJ, Stauffer JA (2012) Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the accordion severity grading system. J Am Coll Surg 215:810–819
10. Zureikat AH, Breaux JA, Steel JL, Hughes SJ (2011) Can laparoscopic pancreaticoduodenectomy be safely implemented? J Gastrointest Surg 15:1151–1157 11. Kendrick ML, Cusati D (2010) Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch Surg 145:19–23 12. Palanivelu C, Rajan PS, Rangarajan M, Vaithiswaran V, Senthilnathan P, Parthasarathi R, Praveen Raj P (2009) Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary Pancreat Surg 16:731–740 13. Gumbs AA, Gayet B (2008) The laparoscopic duodenopancreatectomy: the posterior approach. Surg Endosc 22:539–540 14. Pugliese R, Scandroglio I, Sansonna F, Maggioni D, Costanzi A, Citterio D, Ferrari GC, Di Lernia S, Magistro C (2008) Laparoscopic pancreaticoduodenectomy: a retrospective review of 19 cases. Surg Laparosc Endosc Percutan Tech 18:13–18 15. Dulucq JL, Wintringer P, Mahajna A (2006) Laparoscopic pancreaticoduodenectomy for benign and malignant diseases. Surg Endosc 20:1045–1050 16. Kim SC, Song KB, Jung YS, Kim YH, Park do H, Lee SS, Seo DW, Lee SK, Kim MH, Park KM, Lee YJ (2013) Short-term clinical outcomes for 100 consecutive cases of laparoscopic pylorus-preserving pancreatoduodenectomy: improvement with surgical experience. Surg Endosc 27:95–103 17. Ammori BJ, Ayiomamitis GD (2011) Laparoscopic pancreaticoduodenectomy and distal pancreatectomy: a UK experience and a systematic review of the literature. Surg Endosc 25:2084–2099 18. Gagner M, Pomp A (1997) Laparoscopic pancreatic resection: is it worthwhile? J Gastrointest Surg 1:20–25 19. Lei Z, Zhifei W, Jun X, Chang L, Lishan X, Yinghui G, Bo Z (2013) Pancreaticojejunostomy sleeve reconstruction after pancreaticoduodenectomy in laparoscopic and open surgery. JSLS 17:68–73 20. Kuroki T, Adachi T, Okamoto T, Kanematsu T (2012) A nonrandomized comparative study of laparoscopy-assisted pancreaticoduodenectomy and open pancreaticoduodenectomy. Hepatogastroenterology 59:570–573 21. Nakamura Y, Matsumoto S, Matsushita A, Yoshioka M, Shimizu T, Yamahatsu K, Uchida E (2012) Pancreaticojejunostomy with closure of the pancreatic stump by endoscopic linear stapler in laparoscopic pancreaticoduodenectomy: a reliable technique and benefits for pancreatic resection. Asian J Endosc Surg 5:191–194 22. Suzuki O, Kondo S, Hirano S, Tanaka E, Kato K, Tsuchikawa T, Yano T, Okamura K, Shichinohe T (2012) Laparoscopic pancreaticoduodenectomy combined with minilaparotomy. Surg Today 42:509–513 23. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, Souda H, Gunji H, Miyazaki A, Ikeda A, Tohma T, Matsumoto I (2009) Comparison of laparoscopy-assisted and open pylorus-preserving pancreaticoduodenectomy for periampullary disease. Am J Surg 198:445–449 24. Lee JS, Han JH, Na GH, Choi HJ, Hong TH, You YK, Kim DG (2013) Laparoscopic pancreaticoduodenectomy assisted by minilaparotomy. Surg Laparosc Endosc Percutan Tech 23:e98–e102 25. Boggi U, Signori S, De Lio N, Perrone VG, Vistoli F, Belluomini M, Cappelli C, Amorese G, Mosca F (2013) Feasibility of robotic pancreaticoduodenectomy. Br J Surg 100:917–925 26. Zhan Q, Deng XX, Han B, Liu Q, Shen BY, Peng CH, Li HW (2013) Robotic-assisted pancreatic resection: a report of 47 cases. Int J Med Robot 9:44–51 27. Chalikonda S, Aguilar-Saavedra JR, Walsh RM (2012) Laparoscopic robotic-assisted pancreaticoduodenectomy: a case-matched comparison with open resection. Surg Endosc 26:2397–2402
123
Surg Endosc 28. Lai EC, Yang GP, Tang CN (2012) Robot-assisted laparoscopic pancreaticoduodenectomy versus open pancreaticoduodenectomy—a comparative study. Int J Surg 10:475–479 29. Zhou NX, Chen JZ, Liu Q, Zhang X, Wang Z, Ren S, Chen XF (2011) Outcomes of pancreatoduodenectomy with robotic surgery versus open surgery. Int J Med Robot 7:131–137 30. Giulianotti PC, Sbrana F, Bianco FM, Elli EF, Shah G, Addeo P, Caravaglios G, Coratti A (2010) Robot-assisted laparoscopic pancreatic surgery: single-surgeon experience. Surg Endosc 24:1646–1657 31. Zeh HJ, Zureikat AH, Secrest A, Dauoudi M, Bartlett D, Moser AJ (2012) Outcomes after robot-assisted pancreaticoduodenectomy for periampullary lesions. Ann Surg Oncol 19:864–870 32. Narula VK, Mikami DJ, Melvin WS (2010) Robotic and laparoscopic pancreaticoduodenectomy: a hybrid approach. Pancreas 39:160–164 33. Gumbs AA, Rodriguez Rivera AM, Milone L, Hoffman JP (2011) Laparoscopic pancreatoduodenectomy: a review of 285 published cases. Ann Surg Oncol 18:1335–1341 34. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M; International Study Group on Pancreatic Fistula Definition (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13 35. Horiguchi A, Uyama I, Miyakawa S (2011) Robot-assisted laparoscopic pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci 18:287–291 36. Choi SH, Kang CM, Kim DH, Lee WJ, Chi HS (2011) Robotic pylorus preserving pancreaticoduodenectomy with mini-laparotomy reconstruction in a patient with ampullary adenoma. J Korean Surg Soc 81:355–359 37. Machado MA, Makdissi FF, Surjan RC, Machado MC (2013) Laparoscopic pylorus-preserving pancreatoduodenectomy with double jejunal loop reconstruction: an old trick for a new dog. J Laparoendosc Adv Surg Tech A 23:146–149 38. Kimura Y, Hirata K, Mukaiya M, Mizuguchi T, Koito K, Katsuramaki T (2005) Hand-assisted laparoscopic pylorus preserving pancreaticoduodenectomy for pancreas head disease. Am J Surg 189:734–737 39. Keck T, Kuesters S, Wellner U, Hopt UT, Karcz WK (2011) Laparoscopic pylorus-preserving pancreatic head resection and hybrid open reconstruction via pancreatogastrostomy. J Gastrointest Surg 15:373–377 40. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, Souda H, Gunji H, Miyazaki A, Ikeda A, Tohma T (2009) A totally laparoscopic pylorus preserving pancreaticoduodenectomy and reconstruction. Surg Today 39:359–362 41. Matsuoka L, Parekh D (2012) The minimally invasive approach to surgical management of pancreatic diseases. Gastroenterol Clin North Am 41:77–101 42. Fisher WE, Hodges SE, Wu MF, Hilsenbeck SG, Brunicardi FC (2012) Assessment of the learning curve for pancreaticoduodenectomy. Am J Surg 203:684–690 43. Vaessen C (2011) Location of robotic surgical systems worldwide and in France. J Visc Surg 148:e9–e11 44. Cuschieri A (2000) Laparoscopic hand-assisted surgery for hepatic and pancreatic disease. Surg Endosc 14:991–996 45. Velidedeoglu E, Williams N, Brayman KL, Desai NM, Campos L, Palanjian M, Wocjik M, Bloom R, Grossman RA, Mange K, Barker CF, Naji A, Markmann JF (2002) Comparison of open, laparoscopic, and hand-assisted approaches to live-donor nephrectomy. Transplantation 74:169–172 46. Kaban GK, Czerniach DR, Cohen R, Novitsky YW, Yood SM, Perugini RA, Kelly JJ, Litwin DE (2004) Hand-assisted laparoscopic splenectomy in the setting of splenomegaly. Surg Endosc 18:1340–1343
123
47. Moorthy K, Munz Y, Dosis A, Hernandez J, Martin S, Bello F, Rockall T, Darzi A (2004) Dexterity enhancement with robotic surgery. Surg Endosc 18:790–795 48. Mucksavage P, Kerbl DC, Lee JY (2011) The da VinciÒ surgical system overcomes innate hand dominance. J Endourol 25:1385–1388 49. Maniar HS, Council ML, Prasad SM, Prasad SM, Chu C, Damiano RJ Jr (2005) Comparison of skill training with robotic systems and traditional endoscopy: implications on training and adoption. J Surg Res 125:23–29 50. Heemskerk J, van Gemert WG, de Vries J, Greve J, Bouvy ND (2007) Learning curves of robot-assisted laparoscopic surgery compared with conventional laparoscopic surgery: an experimental study evaluating skill acquisition of robot-assisted laparoscopic tasks compared with conventional laparoscopic tasks in inexperienced users. Surg Laparosc Endosc Percutan Tech 17:171–174 51. Zeh HJ 3rd, Bartlett DL, Moser AJ (2011) Robotic-assisted major pancreatic resection. Adv Surg 45:323–340 52. Sgarbura O, Vasilescu C (2010) The decisive role of the patientside surgeon in robotic surgery. Surg Endosc 24:3149–3155 53. Boggi U, Moretto C, Vistoli F, D’Imporzano S, Mosca F (2009) Robotic suture of a large caval injury caused by endo-GIA stapler malfunction during laparoscopic wedge resection of liver segments VII and VIII en-bloc with the right hepatic vein. Minim Invasive Ther Allied Technol 18:306–310 54. Lee HC, Yun MJ, Goo EK, Bahk JH, Park HP, Jeon YT, Lee SC (2010) Rupture of endotracheal tube cuff during robot-assisted endoscopic thyroidectomy—a case report. Korean J Anesthesiol 59:416–419 55. Strasberg SM, Drebin JA, Mokadam NA, Green DW, Jones KL, Ehlers JP, Linehan D (2002) Prospective trial of a blood supplybased technique of pancreaticojejunostomy: effect on anastomotic failure in the Whipple procedure. J Am Coll Surg 194:746–758 56. La¨msa¨ T, Jin HT, Nordback PH, Sand J, Luukkaala T, Nordback I (2009) Pancreatic injury response is different depending on the method of resecting the parenchyma. J Surg Res 154:203–211 57. Emam TA, Cuschieri A (2003) How safe is high-power ultrasonic dissection? Ann Surg 237:186–191 58. Druzˇijanic´ N, Pogorelic´ Z, Perko Z, Mrklic´ I, Tomic´ S (2012) Comparison of lateral thermal damage of the human peritoneum using monopolar diathermy, Harmonic scalpel and LigaSure. Can J Surg 55:317–321 59. Boggi U, Caniglia F, Amorese G (2014) Laparoscopic robotassisted major hepatectomy. J Hepatobiliary Pancreat Sci 21:3–10 60. Owen RM, Perez SD, Lytle N, Patel A, Davis SS, Lin E, Sweeney JF (2013) Impact of operative duration on postoperative pulmonary complications in laparoscopic versus open colectomy. Surg Endosc 27:3555–3563 61. Evans C, Lim J, Gatzen C, Huang A (2012) Factors influencing laparoscopic colorectal operative duration and its effect on clinical outcome. Surg Laparosc Endosc Percutan Tech 22:437–442 62. Procter LD, Davenport DL, Bernard AC, Zwischenberger JB (2010) General surgical operative duration is associated with increased risk-adjusted infectious complication rates and length of hospital stay. J Am Coll Surg 210:60–65 63. Cameron JL, Riall TS, Coleman J, Belcher KA (2006) One thousand consecutive pancreaticoduodenectomies. Ann Surg 244:10–15 64. Bernard AC, Davenport DL, Chang PK, Vaughan TB, Zwischenberger JB (2009) Intraoperative transfusion of 1 U to 2 U packed red blood cells is associated with increased 30-day mortality, surgical-site infection, pneumonia, and sepsis in general surgery patients. J Am Coll Surg 208:931–937
Surg Endosc 65. Zhang J, Wu WM, You L, Zhao YP (2013) Robotic versus open pancreatectomy: a systematic review and meta-analysis. Ann Surg Oncol 20:1774–1780 66. Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM Jr (2013) A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg 216:1–14 67. Verbeke CS, Leitch D, Menon KV, McMahon MJ, Guillou PJ, Anthoney A (2006) Redefining the R1 resection in pancreatic cancer. Br J Surg 93:1232–1237
68. Esposito I, Kleeff J, Bergmann F, Reiser C, Herpel E, Friess H, Schirmacher P, Bu¨chler MW (2008) Most pancreatic cancer resections are R1 resections. Ann Surg Oncol 15:1651–1660 69. Chun YS, Milestone BN, Watson JC, Cohen SJ, Burtness B, Engstrom PF, Haluszka O, Tokar JL, Hall MJ, Denlinger CS, Astsaturov I, Hoffman JP (2010) Defining venous involvement in borderline resectable pancreatic cancer. Ann Surg Oncol 17:2832–2838
123
