ORIGINAL ARTICLE

Practice Patterns and Perioperative Outcomes of Laparoscopic

Pancreaticoduodenectomy in China
A Retrospective Multicenter Analysis of 1029 Patients
Min Wang, MD,  Bing Peng, MD,y Jianhua Liu, MD,z Xinmin Yin, MD,§ Zhijian Tan, MD,ô Rong Liu, MD,jj
Defei Hong, MD, PhD, FACS,  Wenxing Zhao, MD,yy Heshui Wu, MD,zz Rufu Chen, MD,§§
Downloaded from https://journals.lww.com/annalsofsurgery by 01UGrXh3ipqzR4DKqW7bOJtSxsRVOheLV9OzOeHq2POX2t1GrKUD6m1aBQdlm0lX7bZxxCFBpuxAM3exuxdXARVaPXROhrEIELxLuiE5dAoxEXL1EbBXOmtN5qOe2K0cRH9XYihoqJLhl/QMQTWBWg== on 03/16/2021

Dewei Li, MD,ôô Heguang Huang, MD,jjjj Yi Miao, MD, FACS,  yyy Yahui Liu, MD,zzz
Tingbo Liang, MD,§§§ Wei Wang, MD,ôôô Yunqiang Cai, MD,y Zhongqiang Xing, MD,z
Wei Cheng, MD, FACS,§ Xiaosheng Zhong, MD,ô Zhiming Zhao, MD,jj Jungang Zhang, MD,jjjjjj
Zhiyong Yang, MD,zz Guolin Li, MD,§§ Yue Shao, MD,ôô Guirong Lin, MD,jjjj
Kuirong Jiang, MD, FACS,  yyy Pengfei Wu, MD,  yyy Baoxing Jia, MD,zzz Tao Ma, MD,§§§
Chongyi Jiang, MD,ôôô Shuyou Peng, MD, FACS, and Renyi Qin, MD, FACS 

cantly with surgeons’ experience with the procedure. Univariate and multi-
Objective: The aim of the study was to analyze the outcomes of patients who
variate analyses revealed that the pancreatic anastomosis technique, preoper-
have undergone laparoscopic pancreaticoduodenectomy (LPD) in China.
ative biliary drainage method, and total bilirubin were linked to several
Summary Background Data: LPD is being increasingly used worldwide,
outcome measures, including OT, estimated intraoperative blood loss, and
but an extensive, detailed, systematic, multicenter analysis of the procedure
mortality. Multicenter analyses of the learning curve revealed 3 phases, with
has not been performed.
proficiency thresholds at 40 and 104 cases. Higher hospital, department, and
Methods: We retrospectively reviewed 1029 consecutive patients who had
surgeon volume, as well as surgeon experience with minimally invasive
undergone LPD between January 2010 and August 2016 in China. Univariate
surgery, were associated with a lower risk of surgical failure.
and multivariate analyses of patient demographics, changes in outcome over
Conclusions: LPD is technically safe and feasible, with acceptable rates of
time, technical learning curves, and the relationship between hospital or
morbidity and mortality. Nonetheless, long learning curves, low-volume
surgeon volume and patient outcomes were performed.
hospitals, and surgical inexperience are associated with higher rates of
Results: Among the 1029 patients, 61 (5.93%) required conversion to
complications and mortality.
laparotomy. The median operation time (OT) was 441.34 minutes, and the
major complications occurred in 511 patients (49.66%). There were 21 deaths Keywords: hospital volume, laparoscopic, learning curve, outcomes,
(2.43%) within 30 days, and a total of 61 (5.93%) within 90 days. Discounting pancreaticoduodenectomy
the effects of the early learning phase, critical parameters improved signifi-
(Ann Surg 2021;273:145–153)

From the Department of Biliary–Pancreatic Surgery, Affiliated Tongji Hospital,
Tongji Medical College, Huazhong University of Science and Technology,
Wuhan, Hubei, China; yDepartment of Pancreatic Surgery, West China
Hospital, Sichuan University, Chengdu, Sichuan, China; zDepartment of
Hepato-Pancreato-Biliary Surgery, The Second Hospital of Hebei Medical
University, Shijiazhuang, Hebei, China; §Department of Hepatobiliary Sur-
gery, Hunan Provincial People’s Hospital, The First Affiliated Hospital of
Hunan Normal University, Changsha, Hunan, China; ôDepartment of Hep-
atobiliary and Pancreatic Surgery, Guangdong Provincial Hospital of Chinese
Medicine, Guangzhou, Guangdong, China; jjThe Second Department of
Hepato-Pancreato-Biliary Surgery, Chinese PLA General Hospital, Beijing,
China; Division of General Surgery, Sir Run Run Shaw Hospital (SRRSH),
Affiliated with the Zhejiang University School of Medicine, Hangzhou,
Zhejiang, China; yyDepartment of General Surgery, The Affiliated Hospital
of Xuzhou Medical University, Xuzhou, Jiangsu, China; zzDepartment of
Pancreatic Surgery, Union Hospital, Tongji Medical College, Huazhong
University of Science and Technology, Wuhan, Hubei, China;
§§Department of Pancreaticobiliary Surgery, Sun Yat-sen Memorial Hospital,
Sun Yat-sen University, Guangzhou, China; ôôDepartment of Hepatobiliary
Surgery, The First Affiliated Hospital of Chongqing Medical University,
Chongqing, China; jjjjDepartment of General Surgery, Fujian Medical Uni-
versity Union Hospital, Fuzhou, Fujian, China; Pancreas Center, The First
Affiliated Hospital of Nanjing Medical University, Nanjing, China;
yyyPancreas Center, Nanjing Medical University, Nanjing, Jiangsu, China;
zzzDepartment of Hepatobiliary and Pancreatic Surgery, The First Hospital of
Jilin University, Changchun, Jilin, China; §§§Department of Hepatobiliary and
Pancreatic Surgery, The First Affiliated Hospital, Zhejiang University School
of Medicine, Hangzhou, Zhejiang, China; ôôôDepartment of Surgery,
Huadong Hospital, Fudan University, Shanghai, China; jjjjjjDivision of
Hepatobiliary and Pancreatic Surgery and Minimally Invasive Surgery,
Zhejiang Provincial People’s Hospital, Hangzhou, Zhejiang, China; and
Department of General Surgery, The Second Affiliated Hospital of
Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.
MW, BP, JL, XY, ZT, RL, DH, WZ, HW, RC, DL, HH, YM, YL, TL, and WW
equally contributed to this work.
Minimally Invasive Pancreas Treatment Group in the Pancreatic Disease Branch of
China’s International Exchange and Promotion Association for Medicine and
Healthcare.
Authors’ contributions: MW and RQ were involved in drafting the article and in the
analysis and interpretation of data. BP, JL, XY, ZT, RL, DH, WZ, HW, RC, DL,
HH, YM, KJ, YL, TL, and WW performed the LPD operations and participated
in data collection, analysis, and interpretation. Y.C, ZX, WC, XZ, ZZ, JZ, ZY,
GL, YS, GL, PW, BJ, TM, and CJ participated in data collection. MW, SP, and
RQ were involved in the conception, design, and critical revision of the article
and obtained funding. RQ is the guarantor.
This study was supported by grants from the National Natural Science Foundation
of China (81272659, 81772950, 81773160, 81702792, 81502633, 81602475,
81874205), HUBEI Natural Science Foundation (2017CFB467), and Tongji
Hospital Science Fund for Distinguished Young Scholars (2017).
The authors report no conflicts of interest.
Supplemental digital content is available for this article. Direct URL citations
appear in the printed text and are provided in the HTML and PDF versions of
this article on the journal’s Web site (www.annalsofsurgery.com).
Reprints: Renyi Qin, MD, Department of Biliary–Pancreatic Surgery, Affiliated
Tongji Hospital, Tongji Medical College, Huazhong University of Science and
Technology, 1095 Jiefang Avenue, Wuhan, Hubei 430030, China. E-mail:
ryqin@tjh.tjmu.edu.cn.
Copyright ß 2019 Wolters Kluwer Health, Inc. All rights reserved.
ISSN: 0003-4932/19/27301-0145
DOI: 10.1097/SLA.0000000000003190

Annals of Surgery  Volume 273, Number 1, January 2021 www.annalsofsurgery.com | 145

Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.

Wang et al
P ancreaticoduodenectomy (PD) is one of the most complex
procedures in gastroenterological surgery, requiring extensive
dissection and complex reconstructive anastomoses.1 The first lapa-
roscopic PD (LPD) was described by Gagner in 1994,2 and still
remains a challenging procedure because of the technical limitations
of laparoscopy and the need for advanced laparoscopic skills, which
are associated with long learning curves. Over the past decade, LPD
has been increasingly used worldwide, although the feasibility and
safety of the laparoscopic approach remain controversial.3
Recent comparisons between LPD and open PD (OPD) show
that the 2 approaches do not differ with regard to the incidence of
postoperative morbidity, short-term oncologic outcomes, and long-
term overall survival rates; however, LPD is associated with a lower
estimated intraoperative blood loss (EIBL), shorter length of stay
(LOS), a higher rate of R0 resection, and the harvesting of more
lymph nodes.4 –9 Several other studies have reported substantially
higher rates of postoperative pancreatic fistula (POPF), postpancrea-
tectomy hemorrhage, and 30-day postoperative mortality after LPD
relative to OPD.8,10,11 Despite the ongoing debate about the risks and
benefits of LPD, an increasing number of centers are performing or
planning to adopt this approach, and the number of LPDs performed
each year is rising rapidly.12 Enthusiasm for the procedure continues
to grow at high-volume as well as low-volume hospitals.18 However,
no large-scale, multicenter analyses have been performed to investi-
gate in detail the perioperative outcomes, describe changes in critical
technical steps, or evaluate the parameters that correlate with critical
outcomes.13 Surgeons are known to need a relatively extended
training period to become technically proficient in performing this
challenging operation, and the learning curve for developing LPD
proficiency has been described by several investigators. However,
these reports were based on single-center analyses and showed
significant variation among centers.14– 16 Thus, to promote further
adoption of LPD, it is imperative to undertake learning curve assess-
ments across a larger number of centers.17 Although multiple studies
show that hospital and surgeon volumes are significantly correlated
with PD outcomes,19,20 the relationships between these volumes and
LPD outcomes remain unclear. Further understanding of this rela-
tionship is a critical prerequisite for establishing a safe model to
promote LPD.21,22
Our aim was to describe the national patterns of LPD in China.
We have analyzed short-term outcomes of 1029 patients and scrutinized
the characteristics of the procedure and how it is applied at a population
level. We have also investigated the parameters that correlate with
essential outcomes, learning curve features, and the role of hospital
and surgeon volumes in this large cohort. To the best of our knowledge,
this is the largest series of LPDs to be investigated to date.
METHODS
Study Design and Data Collection
A retrospective review of the institutional databases of 16
high-volume pancreatic centers in China identified 1029 consecutive
patients who underwent LPD between January 2010 and August
2016. Each center had performed  20 LPDs (Supplemental Table 1,
http://links.lww.com/SLA/B557). The study was approved by the
institutional review board at each hospital. Inclusion criteria for
centers were high-volume (>60 PDs/yr) and that each surgeon had
performed >100 PDs over the previous 3 years, and was, thus,
considered to be beyond the learning curve.
Patients
Patients with confirmed or suspected borderline or malignant
pathology of the periampullary region were consecutively and
prospectively scheduled for elective LPD. Patients with potential
146 | www.annalsofsurgery.com
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery  Volume 273, Number 1, January 2021
vascular involvement of the superior mesenteric or portal veins that
were longer than 3 cm on preoperative thin-slice (3 mm) computed
tomography (CT) scans and CT portal venography, those with
excessively large lesions (tumor size 10 cm), those with invasion
of adjacent organs and major vessels, and those with severe cardio-
respiratory or hepatorenal insufficiency were not considered to be
candidates for LPD (Supplemental Table 1, http://links.lww.com/
SLA/B557).
Perioperative Variables and Definitions
For this study, hybrid LPD was defined as a combination of
laparoscopic and robotic approaches, and operation time (OT) as the
time from skin incision or trocar placement to complete skin closure.
EIBL was carefully recorded by the anesthetist using a vacuum
system. LOS was defined as the number of days from admission to
discharge. Morbidity and mortality were defined as any complication
or death, respectively, which occurred during hospitalization or
within 30 days of discharge. Hospital reoperation within 30 days
was recorded, and postoperative morbidity was evaluated according
to the Clavien-Dindo (CD) classification system.23 POPF,24 delayed
gastric emptying,25 biliary leak,26 and postoperative hemorrhage27
were also classified as previously reported. Failure of LPD was
defined as death within 30 days, conversion to laparotomy, and
postoperative complications (CD III). Vessel reconstruction was
defined as any repair or replacement of major vessels during
the surgery.
Statistical Analysis
The characteristics of the overall cohort are described as
means with standard deviations for continuous data, and as percen-
tages for categorical data. Analysis of variance was used for com-
parisons of normally distributed variables, the nonparametric
Kruskal–Wallis test for skewed continuous variables, and the chi-
square and Fisher exact tests for categorical variables. Pairwise
comparisons were performed with a Tukey–Kramer adjustment
for multiple comparisons in post hoc analyses when necessary.
Adjusted analyses were performed with linear or logistic
regression models, with the target variable of interest as a predictor
variable. Variables with P < 0.05 in univariate regression analyses
were further evaluated in multivariate regression analyses. Results of
linear regression analyses are presented as beta-coefficients and 95%
confidence intervals (95% CIs). Logistic regression results are
presented as odds ratios (ORs) and 95% CIs.
The learning curve for LPD was evaluated with the cumulative
sum (CUSUM) and risk-adjusted CUSUM (RA-CUSUM) methods,
as previously described.16 PThe CUSUM of the OT (CUSUMOT) was
defined as CUSUMOT ¼ ni1 ðX i  mÞ, where Xi is an individual
OT, and m is the P mean overall OT. RA-CUSUM was defined as
RA-CUSUM ¼ ni1 ðX i  t Þ þ ð1Þx P i , where Xi ¼ 1 indicates
LPD failure; otherwise, Xi ¼ 0; t represents the observed LPD failure
rate; Pi is the expected rate of LPD failure in each case, and was
calculated from the logistic regression model. All statistical analyses
were performed with SAS, version 9.2 (SAS Institute Inc., Cary, NC).
Reported P values were 2-sided, with P < 0.05 considered to be
statistically significant.
RESULTS
Patient Demographics and Perioperative Outcomes
The study population consisted of 1029 patients that had
undergone LPD at 16 centers in China (mean, 64.3 cases/center;
range, 20–204 cases; Table 1 and Supplemental Table 2, http://
links.lww.com/SLA/B557). There were 571 men (55.49%) and
458 women (44.51%), with a median age of 57.52 years (range,
ß 2019 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery  Volume 273, Number 1, January 2021 Analysis of 1029 LPDs Performed in China

TABLE 1. Major Perioperative Outcomes in Total and Over Time

Total By Year
Number (%)/Mean
Demographics (Minimum–Maximum) 2013 2014 2015 2016 P
No. of cases 64.3 (20.00–204.00) 23 (2.24%) 125 (12.15%) 400 (38.87%) 481 (46.74) 0.008z
Sex (M) 571 (55.49) 9 (39.13) 72 (57.60) 222 (55.50) 268 (55.72) 0.6248z
Age (yrs), mean (SD) 57.52 (13.00–85.00) 52.09 (10.60) 58.78 (11.63) 57.22 (12.62) 57.82 (11.23) 0.1201§
BMI, mean (SD) 21.99 (11.97–47.18) 20.96 (2.62) 21.65 (3.69) 21.66 (3.15) 22.30 (3.35) 0.0198§
Previous abdominal surgery 107 (10.4) 3 (13.04) 10 (8.00) 47 (11.75) 47 (9.77) 0.8693z
Preoperative diagnosis 0.7887z
Pancreatic head mass 462 (44.89) 7 (30.43) 55 (44.00) 178 (44.50) 222 (46.15)
Duodenum mass 237 (23.03) 5 (21.74) 27 (21.60) 93 (23.25) 112 (23.28)
Biliary duct mass 197 (19.15) 6 (26.09) 26 (20.80) 71 (17.75) 94 (19.54)
Ampullary mass 133 (12.93) 5 (21.74) 17 (13.60) 58 (14.50) 53 (11.02)
Operative technique 0.1798y
TLPD 912 (88.63) 19 (82.61) 106 (84.80) 353 (88.47) 434 (90.23)
HALPD 84 (8.16) 4 (17.39) 17 (13.60) 27 (6.77) 36 (7.48)
HLPD 33 (3.21) 0 (0.00) 2 (1.60) 20 (4.76) 11 (2.29)
Conversion to laparotomy 61 (5.93) 4 (17.39) 12 (9.60) 24 (6.00) 21 (4.37) 0.0028z
Operative time (min), mean (SD) 441.34 (300.00–850.00) 463.91 (103.69) 447.67 (135.08) 443.65 (269.54) 409.60 (128.56) 0.0007§
EIBL, mean (SD) 312.07 (100–4000.00) 317.39 (395.89) 313.18 (382.79) 355.38 (473.45) 275.52 (365.56) 0.0037§
Major complications 511 (49.66) 14 (60.86) 70 (56) 197 (49.25) 230 (47.82) 0.024z
Postoperative hemorrhage 128 (12.44) 3 (13.04) 18 (14.40) 55 (13.75) 52 (10.81) 0.1933z
Biliary fistula 50 (4.86) 0 (0.00) 9 (7.20) 24 (6.00) 17 (3.54) 0.1393y
Delayed gastric emptying 172 (16.72) 5 (21.74) 17 (13.60) 75 (18.75) 75 (15.63) 0.0013y
A 140 (13.61) 2 (8.70) 13 (10.40) 61 (15.25) 64 (13.33)
B 25 (2.43) 1 (4.35) 4 (3.20) 11 (2.75) 9 (1.88)
C 7 (0.68) 2 (8.70) 0 (0.00) 3 (0.75) 2 (0.42)
POPF 338 (32.85) 5 (21.74) 45 (33.60) 136 (34.00) 155 (32.3) 0.3236y
A 271 (26.34) 4 (17.39) 31 (24.80) 103 (25.75) 133 (27.71)
B 60 (5.83) 1 (4.35) 11 (8.80) 28 (7.00) 20 (4.17)
C 7 (0.68) 0 (0.00) 0 (0.00) 5 (1.25) 2 (0.42)
TNM stage of malignant 0.2629y
IA 177 (17.2) 4 (17.39) 22 (17.60) 57 (14.25) 94 (19.54)
IB 287 (27.89) 3 (13.04) 32 (25.60) 116 (29.00) 136 (28.27)
IIA 82 (7.97) 3 (13.04) 6 (4.80) 31 (7.75) 42 (8.73)
IIB 265 (25.75) 9 (39.13) 38 (30.4) 92 (22.5) 116 (24.12)
III 2 (0.19) 0 (0.00) 0 (0.00) 1 (0.25) 1 (0.21)
CD stage
<3 811 (78.81) 18 (78.26) 90 (72.00) 324 (81.00) 416 (86.49) 0.0002z
3 218 (21.19) 5 (21.74) 35 (28.00) 76 (19.00) 65 (13.51)
P-LOS, mean (SD) 13.54 (5.00–134.00) 18.40 (10.68) 16.21 (9.80) 14.78 (8.37) 11.60 (7.10) <0.0001§
Reoperation 88 (8.55%) 3 (13.04) 22 (17.60) 52 (13.00) 57 (11.85) 0.1697z
Death at 30 d 25 (2.43) 1 (4.35) 8 (6.40) 12 (3.00) 4 (0.83) 0.0024z
BMI indicates body mass index; CD, Clavien–Dindo classification; EIBL, estimated intraoperative blood loss; HALPD, hand-assisted LPD; HLPD, hybrid LPD; P-LOS,
postoperative length of stay; POPF, postoperative pancreatic fistula; TLPD, total LPD.

Mean (Minimum–Maximum).
yFisher exact test.
zPresent CMH chi-square test.
§Present ANOVA test.

13–85 yrs). Total LPD was performed in 912 patients (88.63%),
hand-assisted LPD in 84 (8.16%), and hybrid LPD in 32 (3.21%).
Conversion to laparotomy was required in 61 patients (5.93%).
The median OT was 441.34 minutes, and the median EIBL was
312.07 mL. The major complications occurred in 511 patients
(49.66%) and included postoperative hemorrhage (n ¼ 128,
12.44%), biliary fistula (n ¼ 50, 4.86%), delayed gastric emptying
(n ¼ 172, 16.72%), POPF (n ¼ 338, 32.85%), abdominal abscess (n
¼ 100, 9.72%), and pulmonary infection (n ¼ 59, 5.73%). As per the
international clinical grading system, the POPF was classified as
grades A, B, or C in 271 (26.34%), 60 (5.83%), and 7 patients
(0.68%), respectively. According to the CD grading system, most
complications were classified as grade 1 or 2. The CD grade 3
complications were occurred in 218 patients (21.19%). The mean
total and postoperative LOS were 20.42 and 13.54 days, respectively.
Reoperation for complications within 30 days was required in 88
patients (8.55%). There were 25 (2.43%) deaths within 30 days,
and 61 (5.93%) within 90 days after LPD. The mean tumor size
was 2.59 cm. The mean number of lymph nodes resected, and the
number of positive nodes were 10.52 and 0.69, respectively. The
rate of clean resection margins was 97.57%. Most patients with
malignant lesions were TNM stage I (n ¼ 464, 45.09%) or II (n ¼
347, 33.72%).
Changes in Outcomes Over the Study Period
Between 2010 and 2016, the annual number of LPD proce-
dures in China steadily rose, with an especially rapid increase after
2013. As the total number of procedures performed before 2013 was

ß 2019 Wolters Kluwer Health, Inc. All rights reserved. www.annalsofsurgery.com | 147

Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.

Wang et al Annals of Surgery  Volume 273, Number 1, January 2021

TABLE 2. Factors Associated With OT and EIBL

UV and MV Analysis of Factors Associated With OT
UVA MVA

Variable b SD P b SD P
Age 0.89 0.315 0.005 0.67 0.302 0.027
BMI 2.939 1.144 0.01 3.346 1.092 0.002
Pancreatic anastomosis (imbedding)
Duct-to-mucosa 63.431 9.149 <0.001 51.188 10.678 <0.001
End-to-end 161.648 19.382 <0.001 133.609 20.205 <0.001
Choledochojejunostomy (combined suture)
Continuous suture 17.559 7.787 0.024 50.438 8.950 <0.001
Interrupted suture 24.931 28.665 0.385 68.064 28.082 0.116
Gastrointestinal anastomosis (hand-sewn)
ENDO-GIA 79.462 11.078 <0.001 52.83 11.36 <0.001

UV and MV Analysis of Factors Associated With EIBL

UVA MVA
Variable b SD P b SD P
Sex (M) 64.299 25.934 0.013 58.467 25.988 0.025
Age 2.602 1.089 0.017 1.930 1.143 0.091
TB 0.103 0.118 0.382 0.273 0.133 0.041
No. of lymphnodes 12.494 2.055 <0.001 13.243 2.236 <0.001
PBD (no)
PTCD 53.246 33.204 0.109 67.429 36.045 0.062
ENBD 181.296 57.629 0.002 167.118 57.730 0.004
Stent 42.340 89.251 0.635 21.305 90.317 0.814

MV analysis with a priori hypothesis.

only 23, we analyzed all data from before this year as a single group
(Supplemental Fig. 1, http://links.lww.com/SLA/B557).
No significant changes were detected over time in most
preoperative patient characteristics, but there was a trend toward
higher body mass index (BMI) and more patients with pancreatic
head masses, suggesting that more challenging cases were handled
later in the learning curve. However, several critical intraoperative
outcomes changed during the period studied. The conversion to
laparotomy rate dropped from 17.39% before 2013 to 4.37% in
2016, the mean OT decreased significantly (463.91 to 409.60 min),
and mean EIBL (317.39 to 275.52 mL) showed a gradual
decline. The rate of complications decreased slightly, from
60.86% to 47.82%, but the hemorrhage, biliary fistula, and overall
POPF rates did not change. However, the incidence of grade B POPF
did decline from 8.80% in 2014 to 4.17% in 2016. The overall CD
grades and rates of reoperation within 30 days did not vary.
However, the rate of complications of CD grade 3 fell from
21.74% to 13.51%. The mean LOS decreased from 26.30 days to
18.46 days, and the mean postoperative LOS fell from 18.40 to 11.60
days. Deaths within 30 days declined markedly, from 6.40% to
0.83%, and the rate of operation failure fell from 34.78% to 17.05%.
The histological classification, mean tumor size, and mean number
of lymph nodes resected, and positive nodes, rate of clean resection
margins, and TNM staging did not change over time (see Table 1;
further details in Supplemental Table 3, http://links.lww.com/SLA/
B557).

FIGURE 1. The learning curves

were assessed for all surgeons
across the entire patient cohort
by average CUSUMOT analysis.

148 | www.annalsofsurgery.com ß 2019 Wolters Kluwer Health, Inc. All rights reserved.

Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.

Annals of Surgery  Volume 273, Number 1, January 2021 Analysis of 1029 LPDs Performed in China

Factors Associated With Intraoperative,
Postoperative, and Oncological Outcomes
Univariate and multivariate analyses were used to identify the
risk factors associated with perioperative outcomes. The factors used
to perform multivariate analyses were selected according to clinical
significance. In addition, we also performed multivariate analyses
without a priori hypotheses to explore some potentially informative
findings, which may have been omitted from a priori hypotheses
(Supplemental Tables 4–13, http://links.lww.com/SLA/B557).
The factors associated with the primary intraoperative out-
comes (OT and EIBL) are shown in Table 2. After adjusting for
confounders, we found advanced age, higher BMI, and duct-to-
mucosa plus end-to-end pancreatic anastomosis to be correlated
with longer OTs, whereas continuous suture choledochojejunostomy
and stapled gastrointestinal anastomosis were associated with shorter
OTs (Supplemental Table 4, http://links.lww.com/SLA/B557). Mul-
tivariate analysis showed that male sex, higher total bilirubin (TB),
higher lymph node yield, and preoperative endoscopic nasal biliary
drainage (ENBD) were correlated with greater volumes of EIBL
(Supplemental Table 5, http://links.lww.com/SLA/B557).
The factors associated with operative safety [clinically rele-
vant POPF (CR-POPF), CD 53 complications, and mortality] are
shown in Table 3. In multivariate analysis, higher BMI, longer OTs,
and preoperative biliary stents were associated with a higher risk of
CR-POPF (Supplemental Table 6, http://links.lww.com/SLA/B557),
whereas pancreatic duct stents were associated with a lower risk of
CR-POPF. Higher lymph node yield and longer OTs were associated
with an increased risk of CD grade 53 complications on multivariate
analysis (Supplemental Table 7, http://links.lww.com/SLA/B557).
After covariable adjustment, older age, higher TB, and TNM stage
were found to be associated with 30-day mortality (Supplemental
Table 8, http://links.lww.com/SLA/B557). Higher TB and T3 tumors
were associated with a higher rate of 90-day mortality. However, the
duct-to-mucosa pancreatic anastomosis was associated with a lower
rate of 90-day mortality (Supplemental Table 9, http://links.lww.
com/SLA/B557).
The factors associated with postoperative LOS and reopera-
tion rate are shown in Supplemental Tables 10 and 11. After adjusting
for confounders, a higher yield of lymph nodes, longer OTs,
greater volumes of EIBL, transfusion, previous abdominal surgery,
hand-assisted LPD, hybrid LPD, higher CD grade, postoperative
nasogastric tube use, CR-POPF, duodenal tumors, and T3 tumors
were independently associated with longer LOS. In contrast, lower
ASA stage and continuous-suture choledochojejunostomy were
independently associated with shorter LOS (Supplemental
Table 10, http://links.lww.com/SLA/B557). CR-POPF was the only
factor associated with a higher reoperation rate on multivariate
analysis (Supplemental Table 11, http://links.lww.com/SLA/B557).
The factors associated with oncologic outcomes are shown in
Supplemental Tables 12 and 13. Multivariate analysis revealed an
association of larger tumor size, malignancy, differentiation, and
TNM stage with higher lymph node yield. Conversely, greater EIBL,
transfusion, ENBD, hybrid LPD, biliary duct cancer, duodenum

TABLE 3. UV and MV Analysis of Factors Associated With CD 53, Death at 30 and 90 days
UV and MV Analysis of Factors Associated With CD 3
UVA MVA
Variable OR (95% CI) P OR (95% CI) P
No. of lymphnodes 1.102 (1.000–1.228) 0.034 1.119 (1.000–1.323) 0.017
Operative time 1.001 (1.000–1.003) 0.043 1.023 (1.000–1.31) 0.023
Gastrointestinal anastomosis (hand-sewn)
ENDO-GIA 0.594 (0.384–0.920) 0.02 0.656 (0.401–1.074) 0.172
Stent of pancreatic duct 1.499 (1.008–2.228) 0.045 1.015 (0.625–1.651) 0.950

UV and MV Analysis of Factors Associated With Death at 30 d

UVA MVA
Variable OR (95% CI) P OR (95% CI) P
Age 1.048 (1.007–1.090) 0.020 1.046 (1.003–1.090) 0.036
TB 1.003 (1.001–1.005) 0.005 1.002 (1.001–1.004) 0.003
TNM stage (benign)
T1N0M0 2.839 (0.859–9.380) 0.087 4.099 (0.939–17.897) 0.061
T2N0M0 3.546 (1.183–10.636) 0.024 4.652 (1.105–19.584) 0.036
T3N0M0 4.184 (1.149–15.231) 0.03 6.171 (1.174–32.445) 0.032
T1N1M0 5.889 (1.009–34.375) 0.049 7.921 (0.991–63.323) 0.051
T2N1M0 2.092 (0.580–7.541) 0.259 2.907 (0.561–15.056) 0.203
T3N1M0 4.637 (1.322–16.269) 0.017 6.988 (1.339–36.457) 0.021
T4N1M0 53.036 (2.795–1006.265) 0.008 40.388 (1.671–976.149) 0.023

UV and MV Analysis of Factors Associated With Death at 90 d

UVA MVA
Variable OR (95% CI) P OR (95% CI) P
TB 1.002 (1.001–1.004) 0.004 1.002 (1.000–1.004) 0.003
Pancreatic anastomosis (imbedding)
Duct-to-mucosa 0.770 (0.466–1.274) 0.143 0.876 (0.483–1.588) 0.005
End-to-end 1.799 (0.744–4.346) 0.757 2.230 (0.886–5.609) 0.52
TNM stage (benign)
T3N0M0 2.677 (1.167–6.141) 0.02 3.640 (1.105–11.990) 0.034
T3N1M0 4.074 (1.898–8.744) <0.0001 5.329 (1.663–17.080) 0.005

ß 2019 Wolters Kluwer Health, Inc. All rights reserved. www.annalsofsurgery.com | 149

Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.

Wang et al
cancer, and ampullary cancer were associated with lower lymph node
yield (Supplemental Table 12, http://links.lww.com/SLA/B557).
Furthermore, after adjusting for confounders, a higher positive lymph
node yield, greater EIBL, and hand-assisted LPD were independently
associated with positive margins (Supplemental Table 13, http://
links.lww.com/SLA/B557).
Learning Curve Analysis
Learning curves were assessed at 13 centers where >30 cases
of LPD were performed by a single surgeon. The learning curve in
terms of OT was represented intuitively and determined by plotting
the outcomes on the CUSUM curve. The CUSUMOT graph (Supple-
mental Fig. 2 and Supplemental Table 14, http://links.lww.com/SLA/
B557) shows that the learning curves at all centers were divided by 2
peaks: at 3 to 49 cases and at 21 to 96 cases. Decreased OT does not
itself signify competence or success. Therefore, we further evaluated
the learning curve using the RA-CUSUM method (Supplemental Fig.
3 and Supplemental Table 14, http://links.lww.com/SLA/B557). The
learning curves at 11 centers were divided by 2 valley points and
those at 2 centers were divided by 1 valley point. The first valley
points were achieved after completion of 9 to 54 cases, and the
second after 29 to 91 cases. To eliminate bias from the single-center
analysis, we used the average CUSUMOT analysis to identify the
learning curve of LPD across all centers. We first ordered the cases at
each center chronologically from the first to the last and subsequently
calculated the mean OT for each case. As only 1 center had
performed >133 cases, and to ensure that 2 centers were included
in each calculation, we used the mean OT for the first 133 cases for
the average CUSUMOT analysis. Using this method, the plot of the
average CUSUMOT revealed 3 phases of the learning process, with
peaks after completion of 40 and 104 cases (Fig. 1).
Comparison of Perioperative Outcomes Among the
3 Consecutive Phases (Supplemental Table 15,
http://links.lww.com/SLA/B557)
Based on the average CUSUMOT analysis, the cases from all
centers were divided into 3 phases. The phase I group contained 555
(53.94%) cases, which included cases 1 to 40 at all centers; the phase
II group contained 344 (33.43%) cases, which included cases 41 to
104; and the phase III group contained 130 (12.63%) cases, which
included case 104 and beyond.
No significant differences in most preoperative characteristics
were detected among the 3 phases. However, several key periopera-
tive outcomes changed as the surgeon’s accumulated experience. The
rate of conversion to laparotomy was significantly lower in phase III
than in phase I (2.31% vs 7.57%, P ¼ 0.0346). The OT significantly
decreased from phase I to phase III (mean OT in phases I, II, and III
was 471.53, 430.51, and 341.13 min, respectively; P < 0.001). The
TABLE 4. The Relationship Between the Volume and the Operation Failed, CD 3
UVA Analysis
Operation failed CD 3
OR (95% CI) P OR (95% CI)
Open PD volume (<200)
200–1000 2.317 (2.033 – 2.245) <0.001 2.533 (1.574–4.076) <0.001
>1000 2.583 (2.465 – 2.707) <0.001 1.325 (0.814–2.157) 0.2815
Minimally invasive surgery (<100)
100–500 0.944 (0.901 – 0.988) <0.001 0.665 (0.443–0.999)
>500 0.941 (0.986 – 0.999) 0.008 0.731 (0.445–1.201)
Annual LPD volume (<20)
20–50 0.971 (0.929–1.014) <0.001 0.991 (0.682–1.467)
>50 0.950 (0.902–0.989) <0.001 0.540 (0.351–0.833)
150 | www.annalsofsurgery.com
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery  Volume 273, Number 1, January 2021
volume of EIBL was significantly lower in phase III (150.0 mL) than
in phase I (200.0 mL, P < 0.0292). The LOS was significantly shorter
after phase II (P < 0.001). The incidence of CR-POPF tended to
decline with increasing experience (P < 0.05), but this trend was not
statistically significant in interphase comparisons with the overall
rate of POPF. There was a significant decline in CD grade 3 with
increased experience [116 (20.90%) in phase I, 46 (13.37%) in phase
II, 11 (10.58%) in phase III; P < 0.01]. The rate of reoperation within
30 days after LPD significantly decreased from phase I to phase III
[66 (11.89%) in phase I, 20 (5.81%) in phase II, and 2 (1.54%) in
phase III; P < 0.001]. The 30-day mortality tended to decline from
3.6% to 0% with increasing experience (P < 0.0198). Operative
failure declined after phase II. More lymph nodes were collected
after the initial learning period, and the rate of positive margins
significantly fell over the 3 phases [17 (3.06%) in phase I, 2 (0.58%)
in phase II, and 0 (0.00%) in phase III; P < 0.0105].
Effect of Hospital Volume, Department Volume,
Surgeon’s Experience, and Surgeon’s Volume on
Patient Outcomes
The surgeon’s volume was defined as the number of LPDs
performed annually. Experience with minimally invasive surgery was
defined as the cumulative number of minimally invasive operations
performed, including laparoscopic gastrointestinal surgery, splenec-
tomy, distal pancreatectomy, and hepatectomy. We used 25% and
75% percentiles to classify volume into the high, medium, and low
groups, as shown in Supplemental Table 16, http://links.lww.com/
SLA/B557. Hospital volume, department volume, and prior experi-
ence of the surgeon with OPD were associated with the operation
failure rate, whereas surgeon’s experience with minimally invasive
procedures and surgeon’s volume were not. OPD experience and
surgeon’s volume were associated with complications of CD grade
3 (Supplemental Table 16, http://links.lww.com/SLA/B557). Uni-
variate analysis revealed that higher hospital and department vol-
umes, experience with minimally invasive surgery, and surgeon’s
volume were associated with a lower risk of operation failure,
whereas OPD volume was associated with a higher risk of operation
failure. In addition, hospital volume (>4000 beds), department
volume (70–200 beds), OPD experience of 200 to 1000 cases per
year, and surgeon’s annual LPD volume were associated with fewer
CD grade 3 complications (Table 4 and Supplemental Table 16,
http://links.lww.com/SLA/B557). Multivariate analysis showed that
higher hospital and department volume, greater experience with
minimally invasive procedures, and surgeon’s volume were associ-
ated with significantly lower risk of operation failure, whereas OPD
experience was not. Only hospital capacity of >4000 beds was
associated with fewer CD grade 3 complications (Table 4 and
Supplemental Table 16, http://links.lww.com/SLA/B557).
MVA Analysis
Operation failed CD 3
P OR (95% CI) P OR (95% CI) P
0.926 (0.833–1.029) 0.0734 0.768 (0.372–1.584) 0.3728
1.083 (0.928–1.264) 0.0993 1.109 (0.387–3.181) 0.6301
0.1078 0.598 (0.526–0.68) <0.0001 1.677 (0.682–4.124) 0.2117
0.5871 0.66 (0.454–0.896) <0.0001 0.874 (0.334–2.283) 0.4229
0.0398 0.768 (0.686–0.86) <0.0001 0.806 (0.385–1.69) 0.1066
0.0004 0.872 (0.493–1.348) <0.0001 0.268 (0.056–1.28) 0.0702
ß 2019 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery  Volume 273, Number 1, January 2021 Analysis of 1029 LPDs Performed in China

TABLE 5. MV Analysis of the Relationship Between Surgeon Experience, Surgeon Volume and the Outcomes of the LPD
Death at 30 d CR-POPF LOS
Variable OR (95% CI) P OR (95% CI) P b SE P
Open PD volume (<200)
200–1000 0.501 (0.341–1.987) 0.52 0.759 (0.343–1.681) 0.1304 8.061 1.424 <0.0001
>1000 0.738 (0.457–2.301) 0.711 1.514 (0.603–3.802) 0.1455 0.113 2.009 0.9553
Minimally invasive surgery (<100)
100–500 1.665 (0.565–4.907) 0.3078 0.614 (0.277–1.362) 0.503 3.338 1.858 0.0727
>500 10.015 (1.140–87.998) 0.0497 0.210 (0.081–0.544) 0.008 5.129 2.053 0.0126
Annual LPD volume (<20)
20–50 1.795 (0.667–4.828) 0.1275 1.794 (0.853–3.772) 0.3349 5.117 1.491 0.0006
>50 0.866 (0.292–2.564) 0.3571 1.724 (0.811–3.665) 0.4426 12.357 3.024 <0.0001

We further explored the relationship of volumes with mortal-
ity, CR-POPF, and LOS. We found that only surgeon’s experience
with minimally invasive procedures was associated with 30-day
mortality, but the relationship between volumes and 90-day mortality
was not observed. Hospital volume, department volume, surgeon’s
volume, and prior experience of the surgeon with OPD and mini-
mally invasive procedures were all associated with the CR-POPF.
Hospital volume, department volume, surgeon’s volume, and prior
experience of the surgeon with OPD were associated with the LOS
(Supplemental Table 17, http://links.lww.com/SLA/B557). Further-
more, the association between volumes and 30-day mortality, CR-
POPF, and LOS was assessed using univariate (Supplemental
Table 18, http://links.lww.com/SLA/B557) and multivariate analy-
ses. After adjusting for confounders, we found that only surgeon’s
experience with minimally invasive procedures (>500) was associ-
ated with a significantly lower risk of 30-day mortality and fewer
CR-POPFs. Higher hospital volume (>4000), higher department
volume (>200), prior experience of the surgeon with OPD (200–
1000), surgeon’s minimally invasive experience (>500), and sur-
geon’s volume were independently associated with shorter LOS
(Table 5 and Supplemental Table 19, http://links.lww.com/SLA/
B557).
DISCUSSION
Our multicenter study is the largest to date in which peri-
operative outcomes, correlation factors, learning curves, and the
relationship between hospital and surgeon volumes and surgical
outcomes of LPD have been investigated. We first evaluated the
perioperative data to determine the efficiency and approach to LPD
in China. We found that some factors related to LPD, including OT
and major complications rate, were equivalent to those of LPD as
reported in the national database. However, a slightly higher fre-
quency of reoperations and 30-day mortalities, and significantly
longer hospital stays were reported for LPD.10,28– 34 Although we
did not perform a direct comparison with OPD data in China, our data
show that mean OT, 30-day mortality, and reoperation rates are
higher for LPD in contrast to reported data for matched OPD cases,
but that the overall rate of major complications is similar.10,34
Furthermore, after removing the effect of the early learning phase,
we found significant improvements in several critical parameters,
including the rate of conversion to laparotomy, OT, volume of EIBL,
and 30-day mortality. For innovative surgical techniques to be
accepted for routine use, confirmation of their safety is of paramount
importance. Adam et al reported that 30-day mortality was signifi-
cantly higher at low-volume centers (<10 LPDs annually) than at
high-volume centers (>10 LPDs).10 In the present study, the 30-day
mortality was higher in the early stages of the surgeons’ experience,
but decreased significantly after the initial learning curve. These
findings indicate that although the introduction of LPD should be
supervised carefully,35 the learning curve is nonetheless surmount-
able. This result should encourage an expansion in the use of LPD.36
Although many studies have addressed the factors associated
with OPD outcomes, few have focused on LPD. The present study is
the first to analyze the relationship between perioperative factors and
critical outcomes of LPD. We found that the pancreatic anastomosis
technique, the preoperative biliary drainage method, TB, postoperative
nasogastric tube decompression, and pancreatic duct stenting were
significantly associated with outcomes. According to our data, duct-to-
mucosa pancreaticojejunostomy (PJ) remains the most widely used
technique in OPD. However, it is associated with longer OTs, greater
volume of EIBL, and longer LOS than other methods, despite a lower
90-day readmission rate. The LPD procedure is technically challeng-
ing and necessitates accurate needle handling and prevention of suture
tangling in a nondilated pancreatic duct and soft pancreas. Several LPD
techniques have been reported, but the optimal approach is unclear.37–
40
The different techniques of reconstructing the remnant pancreas in
LPD should also be compared in future studies, with a focus on 2
approaches: (1) PJ without suturing the pancreatic duct, which is used
in the modified end-to-side (imbedding) pancreatic anastomosis and
may reduce the OT; and (2) sealing the pancreatic remnant with the
jejunum, which is used in the duct-to-mucosa PJ and may reduce the
90-day readmission rate.37–40 These findings suggest that studies of
new anastomotic approaches in LPD should focus on suturing without
seaming the pancreatic duct directly and avoiding direct exposure of
the remnant pancreas to the jejunum.
Preoperative biliary drainage in OPD has also been very
controversial.41,42 We showed that high TB is associated with higher
rates of 30-day as well as 90-day mortality, and that ENBD is
associated with a higher volume of EIBL and lower lymph node
yield. This raises questions about the benefits of preoperative biliary
drainage before LPD and the optimal method. Our data do not
support a recommendation for routine ENBD. The routine use of
postoperative nasogastric tube retention in OPD is still disputed, but
it is another factor related to several essential outcomes.43,44
Although we cannot firmly conclude that routine postoperative
nasogastric decompression adversely impacts the postoperative
course after LPD, the number of patients receiving a nasogastric
tube declined over the course of our study. Furthermore, several
indicators of increased adoption of enhanced recovery after surgery
(ERAS) pathways, such as earlier first oral intake, earlier postoper-
ative activity time, and more postoperative analgesia, were also
observed over the study period. Few reports exist on a special ERAS
pathway for LPD; however, given the minimally invasive nature of
LPD, a validated ERAS pathway would of greater benefit in LPD
than OPD. Further analysis of factors associated with the periopera-
tive outcome is required to reduce the risks associated with LPD.
Although several earlier studies have evaluated the learning
curve for LPD, they were limited by their single-center designs and

ß 2019 Wolters Kluwer Health, Inc. All rights reserved. www.annalsofsurgery.com | 151

Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.

Wang et al
small sample sizes.15,16,45 We have observed considerable differ-
ences in outcomes at each center according to the learning stage. The
learning curve tends to be longer at high LPD volume hospitals,
indicating that sample size may skew learning curve analysis. To
reduce such bias, we evaluated the mean OT for each case according
to its chronological order at each center. Our data show that the 40th
and 104th cases were the points at which competence in performing
LPD was achieved. To our knowledge, this is the first study to
objectively determine the learning curve in a multicenter analysis for
LPD. Furthermore, our data show that the learning curve is signifi-
cantly longer than previously reported in single-center analyses. This
information will allow centers that are introducing the LPD proce-
dure to learn from previous experiences, and move through the
learning curve as safely as possible.
Given the rising interest in the use of LPD at high-volume
hospitals, some low-volume hospitals worldwide have also started to
introduce, or are planning to introduce, LPD.18 Numerous studies
have shown that hospital volume is strongly and inversely correlated
with the incidence of postoperative mortality.17 Adam et al recently
reported that hospital volume is significantly associated with out-
comes of LPD, with a threshold of 22 cases per year.21 In addition,
Conrad et al have shown that the higher mortality rates in low-
volume hospitals are associated with the LPD approach.22 Here, we
highlight that not only higher hospital volume, but also higher
department volume and greater surgeon experience with minimally
invasive surgery and LPD are associated with a lower risk of
operation failure. Unexpectedly, univariate analysis revealed that
greater experience with OPD is associated with a higher risk of
operation failure. Although multivariate analysis showed that this
difference is not significant, it is possible that surgeons attempt to
directly mimic their open approach during LPD, giving rise to
adverse effects. This leads us to conclude that surgeons who are
experienced with OPD should, nevertheless, have to undergo strict
training in minimally invasive procedures before undertaking LPD.
Meanwhile, the criteria for credentialing surgeons to perform LPD
should include experience not only with OPD, but also with mini-
mally invasive surgery in general.
Although this study is an extensive and detailed analysis of the
adoption of LPD in China, it still has some limitations. First, the
health care system in China has several distinctive characteristics,
such as massive hospital and department volume, which are rare
elsewhere and may limit the applicability of our volume analysis to
other countries. Second, the study has not compared LPD and OPD
data during the same period in China. However, rather than focus on
specific details, we wish to emphasize that the adoption of LPD
should only occur after careful consideration to avoid harm to
patients. Given the ongoing debate regarding the safe implementa-
tion of this complicated procedure and the current shift toward value-
based health care reimbursement models, our findings are relevant
and timely.
In summary, this extensive, multi-institutional study demon-
strated that LPD is safe, and that it is feasible to expand its use in the
future. However, our findings also highlight that the initial learning
curve, low-volume hospitals, and lack of surgical experience are
associated with higher rates of complications and mortality after
LPD. This report thus serves as a foundation for national protocols
aimed at safer implementation of LPD. Larger prospective cohort
series and prospective randomized studies in multiple countries are
warranted to further validate our outcomes.
ACKNOWLEDGMENTS
The authors thank TingTing Qin, PhD, from the Department of
Epidemiology and Biostatistics, School of Public Health, Tongji
Medical College, Huazhong University of Science and Technology,
152 | www.annalsofsurgery.com
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery  Volume 273, Number 1, January 2021
for her statistical support, and also thank Ms. Sonal Jhaveri and
Editage (www.editage.com) for English language editing.
REFERENCES
1. Cameron JL, Riall TS, Coleman J, et al. One thousand consecutive pancrea-
ticoduodenectomies. Ann Surg. 2006;244:10–15.
2. Gagner M, Pomp A. Laparoscopic pylorus-preserving pancreatoduodenec-
tomy. Surg Endosc. 1994;8:408–410.
3. de Rooij T, Klompmaker S, Abu Hilal M, et al. Laparoscopic pancreatic
surgery for benign and malignant disease. Nat Rev Gastroenterol Hepatol.
2016;13:227–238.
4. Croome KP, Farnell MB, Que FG, et al. Total laparoscopic pancreaticoduo-
denectomy for pancreatic ductal adenocarcinoma: oncologic advantages over
open approaches? Ann Surg. 2014;260:633–638.
5. Langan RC, Graham JA, Chin AB, et al. Laparoscopic-assisted versus open
pancreaticoduodenectomy: early favorable physical quality-of-life measures.
Surgery. 2014;156:379–384.
6. Chalikonda S, Aguilar-Saavedra JR, Walsh RM. Laparoscopic robotic-
assisted pancreaticoduodenectomy: a case-matched comparison with open
resection. Surg Endosc. 2012;26:2397–2402.
7. Song KB, Kim SC, Hwang DW, et al. Matched case-control analysis compar-
ing laparoscopic and open pylorus-preserving pancreaticoduodenectomy in
patients with periampullary tumors. Ann Surg. 2015;262:146–155.
8. Dokmak S, Fteriche FS, Aussilhou B, et al. Laparoscopic pancreaticoduode-
nectomy should not be routine for resection of periampullary tumors. J Am
Coll Surg. 2015;220:831–838.
9. Chen K, Pan Y, Liu XL, et al. Minimally invasive pancreaticoduodenectomy
for periampullary disease: a comprehensive review of literature and meta-
analysis of outcomes compared with open surgery. BMC Gastroenterol.
2017;17:120.
10. Adam MA, Choudhury K, Dinan MA, et al. Minimally invasive versus open
pancreaticoduodenectomy for cancer: practice patterns and short-term out-
comes among 7061 patients. Ann Surg. 2015;262:372–377.
11. Sharpe SM, Talamonti MS, Wang CE, et al. Early national experience with
laparoscopic pancreaticoduodenectomy for ductal adenocarcinoma: a com-
parison of laparoscopic pancreaticoduodenectomy and open pancreaticoduo-
denectomy from the national cancer data base. J Am Coll Surg. 2015;221:
175–184.
12. Ricci C, Casadei R, Taffurelli G, et al. Minimally invasive pancreaticoduo-
denectomy: what is the best ‘‘choice’’? A systematic review and network meta-
analysis of non-randomized comparative studies. World J Surg. 2018;42:788–805.
13. Palanivelu C, Senthilnathan P, Sabnis SC, et al. Randomized clinical trial of
laparoscopic versus open pancreatoduodenectomy for periampullary tumours.
Br J Surg. 2017;104:1443–1450.
14. Liao CH, Liu YY, Wang SY, et al. The feasibility of laparoscopic pancrea-
ticoduodenectomy—a stepwise procedure and learning curve. Langenbecks
Arch Surg. 2017;402:853–861.
15. Lu C, Jin W, Mou YP, et al. Analysis of learning curve for laparoscopic
pancreaticoduodenectomy. J Vis Surg. 2016;2:145.
16. Wang M, Meng L, Cai Y, et al. Learning curve for laparoscopic pancreati-
coduodenectomy: a CUSUM analysis. J Gastrointest Surg. 2016;20:924–935.
17. Tran TB, Dua MM, Worhunsky DJ, et al. The first decade of laparoscopic
pancreaticoduodenectomy in the United States: costs and outcomes using the
nationwide inpatient sample. Surg Endosc. 2016;30:1778–1783.
18. van Hilst J, de Rooij T, Abu Hilal M, et al. Worldwide survey on opinions
and use of minimally invasive pancreatic resection. HPB (Oxford). 2017;
19:190–204.
19. Hata T, Motoi F, Ishida M, et al. Effect of hospital volume on surgical
outcomes after pancreaticoduodenectomy: a systematic review and meta-
analysis. Ann Surg. 2016;263:664–672.
20. Enomoto LM, Gusani NJ, Dillon PW, et al. Impact of surgeon and hospital
volume on mortality, length of stay, and cost of pancreaticoduodenectomy. J
Gastrointest Surg. 2014;18:690–700.
21. Adam MA, Thomas S, Youngwirth L, et al. Defining a hospital volume
threshold for minimally invasive pancreaticoduodenectomy in the United
States. JAMA Surg. 2017;152:336–342.
22. Kutlu OC, Lee JE, Katz MH, et al. Open pancreaticoduodenectomy case
volume predicts outcome of laparoscopic approach: a population-based
analysis. Ann Surg. 2018;267:552–560.
23. Baker MS, Sherman KL, Stocker SJ, et al. Using a modification of the
Clavien-Dindo system accounting for readmissions and multiple interven-
tions: defining quality for pancreaticoduodenectomy. J Surg Oncol.
2014;110:400–406.
ß 2019 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery  Volume 273, Number 1, January 2021
24. Bassi C, Marchegiani G, Dervenis C, et al. The 2016 update of the Interna-
tional Study Group (ISGPS) definition and grading of postoperative pancreatic
fistula: 11 Years After. Surgery. 2017;161:584–591.
25. Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after
pancreatic surgery: a suggested definition by the International Study Group of
Pancreatic Surgery (ISGPS). Surgery. 2007;142:761–768.
26. Koch M, Garden OJ, Padbury R, et al. Bile leakage after hepatobiliary and
pancreatic surgery: a definition and grading of severity by the International
Study Group of Liver Surgery. Surgery. 2011;149:680–688.
27. Wente MN, Veit JA, Bassi C, et al. Postpancreatectomy hemorrhage (PPH): an
International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery.
2007;142:20–25.
28. Kim SC, Song KB, Jung YS, et al. Short-term clinical outcomes for 100
consecutive cases of laparoscopic pylorus-preserving pancreatoduodenec-
tomy: improvement with surgical experience. Surg Endosc. 2013;27:95–103.
29. Asbun HJ, Stauffer JA. Laparoscopic vs open pancreaticoduodenectomy:
overall outcomes and severity of complications using the Accordion Severity
Grading System. J Am Coll Surg. 2012;215:810–819.
30. Gumbs AA, Croner R, Rodriguez A, et al. 200 consecutive laparoscopic
pancreatic resections performed with a robotically controlled laparoscope
holder. Surg Endosc. 2013;27:3781–3791.
31. Stauffer JA, Coppola A, Villacreses D, et al. Laparoscopic versus open
pancreaticoduodenectomy for pancreatic adenocarcinoma: long-term results
at a single institution. Surg Endosc. 2017;31:2233–2241.
32. Conrad C, Basso V, Passot G, et al. Comparable long-term oncologic outcomes
of laparoscopic versus open pancreaticoduodenectomy for adenocarcinoma: a
propensity score weighting analysis. Surg Endosc. 2017;31:3970–3978.
33. Zenoni SA, Arnoletti JP, de la Fuente SG. Recent developments in surgery:
minimally invasive approaches for patients requiring pancreaticoduodenec-
tomy. JAMA Surg. 2013;148:1154–1157.
34. Nassour I, Wang SC, Christie A, et al. Minimally invasive versus open
pancreaticoduodenectomy: a propensity-matched study from a national cohort
of patients. Ann Surg. 2018;268:151–157.
ß 2019 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.
Analysis of 1029 LPDs Performed in China
35. Hogg ME, Besselink MG, Clavien PA, et al. Training in minimally invasive
pancreatic resections: a paradigm shift away from ‘‘See one, Do one, Teach
one’’. HPB (Oxford). 2017;19:234–245.
36. Baker MS, Sharpe SM, Talamonti MS, et al. The learning curve is surmount-
able: in reply to Fong and colleagues. J Am Coll Surg. 2016;222:210–211.
37. Wang M, Xu S, Zhang H, et al. Imbedding pancreaticojejunostomy used in
pure laparoscopic pancreaticoduodenectomy for nondilated pancreatic duct.
Surg Endosc. 2017;31:1986–1992.
38. Shubert CR, Wagie AE, Farnell MB, et al. Clinical risk score to predict
pancreatic fistula after pancreatoduodenectomy: independent external valida-
tion for open and laparoscopic approaches. J Am Coll Surg. 2015;221:
689–698.
39. Poves I, Morato O, Burdio F, et al. Laparoscopic-adapted Blumgart pancrea-
ticojejunostomy in laparoscopic pancreaticoduodenectomy. Surg Endosc.
2017;31:2837–2845.
40. Kim EY, Hong TH. Total laparoscopic pancreaticoduodenectomy using a new
technique of pancreaticojejunostomy with two transpancreatic sutures with
buttresses. J Laparoendosc Adv Surg Tech A. 2016;26:133–139.
41. Iacono C, Ruzzenente A, Campagnaro T, et al. Role of preoperative biliary
drainage in jaundiced patients who are candidates for pancreatoduodenectomy
or hepatic resection: highlights and drawbacks. Ann Surg. 2013;257:191–204.
42. Lai EC, Lau SH, Lau WY. The current status of preoperative biliary drainage
for patients who receive pancreaticoduodenectomy for periampullary carci-
noma: a comprehensive review. Surgeon. 2014;12:290–296.
43. Park JS, Kim JY, Kim JK, et al. Should gastric decompression be a routine
procedure in patients who undergo pylorus-preserving pancreatoduodenec-
tomy? World J Surg. 2016;40:2766–2770.
44. Kunstman JW, Klemen ND, Fonseca AL, et al. Nasogastric drainage may be
unnecessary after pancreaticoduodenectomy: a comparison of routine vs
selective decompression. J Am Coll Surg. 2013;217:481–488.
45. Kuroki T, Kitasato A, Adachi T, et al. Learning curve for laparoscopic
pancreaticoduodenectomy: a single surgeon’s experience with consecutive
patients. Hepatogastroenterology. 2014;61:838–841.
www.annalsofsurgery.com | 153