International Journal of Surgery 103 (2022) 106686

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International Journal of Surgery

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Review

Splenic vessels preserving versus Warshaw technique in spleen preserving

distal pancreatectomy: A systematic review and meta-analysis
Kuan Hang a, +, Lili Zhou a, +, Haoheng Liu b, Yang Huang b, Hao Zhang a, Chunlu Tan a,
Junjie Xiong a, **, 1, Kezhou Li a, *, 1
a
Department of Pancreatic Surgery, West China Hospital, Sichuan University, No. 37, Guoxue Alley, Chengdu, 610041, Sichuan Province, China
b
College of Medicine, Southwest Jiaotong University, Chengdu, 610000, Sichuan Province, China

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Spleen-preserving distal pancreatectomy is widely used to remove benign or low-grade malignant
Spleen-preserving distal pancreatectomy neoplasms located in the pancreatic body and tail. Both splenic vessels preserving (SVP-DP) and splenic vessels
Splenic vessels preservation ligating (Warshaw technique [WT]) distal pancreatectomy are safe and effective methods but which technique is
Warshaw technique
superior remains controversial. Thus, this study aimed to evaluate the clinical outcomes of patients who un­
Postoperative complications
derwent both methods.
Material and methods: Major databases, including PubMed, Embase, Science Citation Index Expanded, and The
Cochrane Library, were searched for studies comparing SVP-DP and the WT for spleen-preserving distal
pancreatectomy up to December 2021. The perioperative and postoperative outcomes were compared between
the SVP-DP and WT groups. Pooled odds ratios (ORs) and weighted mean differences (WMDs) with 95% con­
fidence intervals (CIs) were calculated using fixed- or random-effects models.
Results: Twenty retrospective studies with 2173 patients were analyzed. A total of 1467 (67.5%) patients un­
derwent SVP-DP, while 706 (32.5%) patients underwent WT. Patients in the SVP-DP group had a significantly
lower rate of splenic infarction (OR: 0.17; 95% CI, 0.11–0.25; P < 0.00001) and incidence of gastric varices (OR:
0.19; 95% CI, 0.11–0.32; P < 0.00001) compared to the patients in the WT group; furthermore, they had a
shorter length of hospital stay (WMD: 0.71; 95% CI, − 1.13 to − 0.29; P = 0.0008). There were no significant
differences between the two groups in terms of major complication, postoperative pancreatic fistula (B/C),
reoperation, blood loss, or operation time.
Conclusions: Compared to WT, SVP-DP should be preferred to reduce splenic infarction and gastric varices, and
WT may be more suitable for large tumors. Moreover, considering the shortcomings of retrospective study, a
multicenter randomized controlled study with a large sample size should be conducted to verify our results.

1. Introduction
For patients with malignant neoplasms in the pancreatic body and
tail, distal pancreatectomy (DP) with splenectomy is adopted to achieve
en bloc resection with adequate oncologic margins and lymph node
clearance [1]. However, studies have suggested that resection of the
spleen should be avoided when the pancreatic neoplasm is benign or
low-grade malignant [2], as it plays an important role in the immune
system [3], and splenectomy may increase the risk of developing severe
complications [4–7] such as thrombocytosis, thrombosis, cancer risk,
and overwhelming post-splenectomy infection. To avoid these sequelae,
surgeons have begun to perform spleen-preserving distal pancreatec­
tomy (SPDP). It was first described by Mallet-Guy and Vachon [8] in
1943. The splenic artery and vein were preserved by careful separation
and ligation of the small pancreatic tributaries. Later, in 1988, Warshaw
[9] developed an SPDP technique that included ligation of the splenic

* Corresponding author.
** Corresponding author. Department of Pancreatic Surgery, West China Hospital, Sichuan University, No. 37, Guoxue Alley, Chengdu, 610041, Sichuan Province,
China.,
E-mail addresses: junjiex2011@126.com (J. Xiong), huaxipancreas@163.com (K. Li).
+
These authors contributed equally to this work.
1
These authors were the co-corresponding author.

https://doi.org/10.1016/j.ijsu.2022.106686
Received 25 February 2022; Received in revised form 8 May 2022; Accepted 11 May 2022
Available online 20 May 2022
1743-9191/© 2022 IJS Publishing Group Ltd. Published by Elsevier Ltd. All rights reserved.
K. Hang et al.
Fig. 1. PRISMA flow diagram depicting the process of identification and inclusion of selected.
studies.
vessels while preserving the short gastric and left gastroepiploic vessels.
This technique soon became popular owing to its simplicity, low intra­
operative blood loss, and short operative time. However, the incidence
of postoperative splenic infarction and gastric varices remains high [10,
11]. Another SPDP technique was described by Kimura et al. [12] in
1996. In this technique, the splenic artery and vein were conserved with
careful ligation of the multiple small, short vascular connections to the
body and tail of the pancreas, assuring increased blood supply to the
spleen. In the last two decades, minimally invasive distal pancreatec­
tomy (MIDP) has been widely reported in the literature [13], including
laparoscopic spleen-preserving distal pancreatectomy (LSPDP) and
robot-assisted spleen-preserving distal pancreatectomy (RSPDP), owing
to its cosmetic results, reduced postoperative pain, and enhanced post­
operative recovery. Patients with benign or borderline malignant neo­
plasms can benefit from both techniques, but the superiority of these
techniques remains controversial.
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International Journal of Surgery 103 (2022) 106686
The present study aimed to compare the clinical outcomes of patients
who underwent SPDP with spleen-preserving distal pancreatectomy
(SVP-DP) and Warshaw technique (WT) via laparoscopic, robot-assisted,
and open surgery.
2. Methods
2.1. Data sources and search strategy
Major public medical and scientific databases, including PubMed,
Embase, Science Citation Index Expanded, and The Cochrane Library,
were searched for studies published in English comparing SVP-DP with
WT up to December 2021. Medical subject headings and keywords were
used in all possible combinations as follows: “distal pancreatectomy,”
“left pancreatectomy,” “splenectomy,” “spleen preserving,” “spleen
preserved,” “vessels preservation,” “Warshaw,” “Warshaw’s,”
K. Hang et al. International Journal of Surgery 103 (2022) 106686

Table 1
Study characteristics and quality assessment.
Authors Year Country Study design Approach Type of surgery No. Of patients NOS score

Baldwin et al. 2011 USA Retrospective cohort Lap SVP-DP 5 *****

WT 4
Beane et al. 2011 USA Retrospective cohort Lap/Rob/Open SVP-DP 45 ********
WT 41
Butturini et al. 2012 Italy Retrospective cohort Lap SVP-DP 36 *******
WT 7
Hwang et al. 2013 Korea Retrospective cohort Rob SVP-DP 17 ******
WT 4
Adam et al. 2013 France Retrospective cohort Lap SVP-DP 55 ********
WT 85
Matsushima et al. 2014 Japan Retrospective cohort Lap SVP-DP 7 *******
WT 17
Worhunsky et al. 2014 USA Retrospective cohort Lap SVP-DP 19 *******
WT 31
Zhou et al. 2014 China Retrospective cohort Lap SVP-DP 206 ********
WT 40
Boselli et al. 2015 Italy Retrospective cohort Lap/Rob/Open SVP-DP 5 *****
WT 3
Lee et al. 2016 Singapore Retrospective cohort Lap/Rob SVP-DP 63 *******
WT 26
Nakamura et al. 2016 Japan Retrospective cohort Lap SVP-DP 11 ********
WT 6
Dai et al. 2017 China Retrospective cohort Lap SVP-DP 103 ********
WT 23
Suzumura et al. 2017 Japan Retrospective cohort Lap SVP-DP 14 ******
WT 5
Paiella et al. 2019 Italy Retrospective cohort Lap/Rob/Open SVP-DP 109 ********
WT 55
Wang et al. 2019 China Retrospective cohort Lap SVP-DP 18 ******
WT 17
Yohanathan et al. 2020 USA Retrospective cohort Lap/Open SVP-DP 19 *********
WT 63
Korrel et al. 2021 Europe Retrospective cohort Lap/Rob SVP-DP 634 *********
WT 244
Esposito et al. 2021 Italy Retrospective cohort Rob SVP-DP 24 *******
WT 10
Kim et al. 2021 Korea Retrospective cohort Lap SVP-DP 50 ******
WT 15
Lin et al. 2021 China Retrospective cohort Rob SVP-DP 41 *********
WT 11

Lap = laparoscopic, Rob = robot assisted, SVP-DP = splenic vessels preserving distal pancreatectomy, WT= Warshaw technique, NOS= Newcastle-Ottawa Scale.

“Warshaw’s procedure,” “Warshaw’s technique,” “Kimura,” “Kimura’s,” 2.3. Outcomes

“Kimura’s technique,” “Kimura’s procedure,” “laparoscopic,” “robot,”
“robotic,” “robot-assisted,” and “minimally invasive.” The reference lists
of the selected articles were further examined to identify relevant arti­
cles during the initial search. Only comparative clinical studies with full-
text descriptions were included in the meta-analysis. The final inclusion
of articles was determined by the consensus of the three authors. This
systematic review was conducted in accordance with the Preferred
Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)
statement [14] and AMSTAR (Assessing the Methodological Quality of
Systematic Reviews) guidelines [15]. Our protocol was registered on the
International Platform of Registered Systematic Review and
Meta-analysis Protocols database (INPLASY2021120108) and Research
Registry (reviewregistry1343).
2.2. Inclusion and exclusion criteria
The inclusion criteria were as follows: human studies; SPDP per­
formed on patients with benign or low-grade malignant tumors in the
distal pancreas; studies reporting at least one outcome of interest as
defined next; and in cases in which multiple studies were reported by the
same institute and/or authors, only the higher quality or most recent
study was included in the analysis.
The exclusion criteria were abstracts, letters, editorials, reviews or
guidelines, case reports, non-comparative studies, and studies without
data of interest or data that could not be extracted.
The primary outcome was the incidence of postoperative splenic
infarction [16]. The secondary outcomes were gastric varices [17],
major complication (Clavien–Dindo III-V complication [18]), clinically
related postoperative pancreatic fistula (POPF, ISGPF grades B and C
[19]), reoperation and tumor size. Other outcomes of interest, including
age, sex ratio (M/F), American Society of Anesthesiologists, body mass
index, histopathological diagnosis, blood loss, operation time and hos­
pital stay were also analyzed.
2.4. Data extraction and quality assessment
Data were extracted by two independent observers. The recorded
data included the characteristics of the included studies, patient baseline
parameters, intraoperative outcomes, and postoperative outcomes. The
means and standard deviations of the outcomes were used for the meta-
analysis, unless otherwise mentioned. Methodologies for estimating
means and standard deviations from medians, IQRs, and ranges were
described by Wan et al. [20] and Luo et al. [21]. The Newcastle–Ottawa
Scale (NOS) was used to assess the quality of each study [22], and a score
≥7 stars was regarded as high-quality.
2.5. Statistical analysis
Review Manager Version 5.4 software (Version 5.4.1 for Windows,
The Cochrane Collaboration, 2020) was used to conduct the meta-

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K. Hang et al. International Journal of Surgery 103 (2022) 106686

Table 2
Baseline parameters of patients.
Authors Type of Age Gender BMI ASA Tumor size Histopathological diagnosis(%)
surgery M/F (mm)

Baldwin et al. SVP 81(71–92) NA NA NA NA AC(20), I(60), CP(0), N(20), SCA(0)

WT 81(71–92) NA NA NA NA AC(0), I(50), CP(25), N(0), SCA(25)
Beane et al. SVP 53.4 10/35 NA 2.66 NA I(31), Cystic disease(20), CP(24), N(11), AC(4), O(9)
WT 56.7 19/22 NA 2.78 NA I(27), Cystic disease(32), CP(22), N(12), AC(0), O(7)
Butturini et al. SVP 47.1 ± 7/29 NA NA 25(5–80) SCA(36.1), M(16.7), MCAC(2.8), I(5.6), SPN(8.3), N(19.4), O(11.1)
WT 17.5 1/6 NA NA 25(10–50) SCA(14.3), M(42.9), MCAC(0), I(0), SPN(14.3), N(28.5), O(0)
44.3 ±
17.2
Hwang et al. SVP 43.7 ± 7/10 23.4 NA 30 ± 12 NA
WT 15.1 0/4 21.8 NA 37 ± 21 NA
36.8 ±
10.1
Adam et al. SVP 52.9 ± 11/44 25.1 2.1 33.6 ± 19.7 Cystic disease(32.7), N(38.2), SPN(9.1), I(3.6), CP(14.5), PDAC(1.8), O(0)
WT 12.2 10/75 24.9 1.9 42.5 ± 29.9 Cystic disease(41.2), N(27), SPN(2.3), I(23.5), CP(0), PDAC(0), O(5.9)
56.9 ±
13.1
Matsushima SVP 70(50–86) 4/3 22.8 NA 15(10–40) I(14.3), M(14.3), SPN(14.3), SCN(0), CP(14.3), Metastasis(14.3), O(28.5)
et al. WT 49(30–83) 3/14 22.3 NA 50(13–120) I(17.6), M(23.5), SPN(17.6), SCN(11.8), CP(5.9), Metastasis(11.8), O(11.8)
Worhunsky et al. SVP 56 ± 11 9/10 27.9 2.4 16(5–105) NA
WT 54 ± 15 7/24 26.7 2.3 20(5–100) NA
Zhou et al. SVP 49.9 ± 63/143 23.3 NA 28 ± 15 N(15),M(15.4),SCN(20.4),I(26.2), SPN(14.5), CP(2.4), Cyst(3.3), PC(0.4),
WT 13.7 5/35 23.1 NA 45 ± 26 O(2.4)
46.6 ± N(2.5), M(37.5), SCN(7.5), I(12.5), SPN(30), CP(5), Cyst(5), PC(5), O(0)
12.4
Boselli et al. SVP 46(34–73) 5/3 NA NA NA NA
WT 5/3 NA NA NA NA
Lee et al. SVP 52(16–78) 24/39 NA 1.44 25(10–140) I(20.6), SPN(22.2), M(9.5), SCA(12.7), N(22.2), O(12.7)
WT 51(20–78) 5/21 NA 1.62 34(20–60) I(11.5), SPN(19.2), M(38.5), SCA(7.7), N(11.5), O(11.5)
Nakamura et al. SVP 42.7 ± 5/6 22.9 1.5 25.7 ± 14.9 Cystic disease(54.5), N(27.3), CP(0), Metastasis(18.2)
WT 22.8 4/2 25.2 1.8 46.5 ± 31.2 Cystic disease(50), N(16.7), CP(33.3), Metastasis(0)
58.8 ±
17.9
Dai et al. SVP 43.1 ± 20/83 23.7 1.56 34.9 ± 18.3 SCN(24.3), M(19.4), N(28.2), SPN(18.4), I(1.9), PC(4.9), CP(0), AS(1), O
WT 13.9 6/17 22.8 1.61 43.6 ± 20 (1.9)
50.5 ± SCN(22), M(26), N(13), SPN(30), I(4), PC(4), CP(0), AS(0), O(0)
14.9
Suzumura et al. SVP 56 (19–87) 5/9 20.4 NA 22(8–84) N(50), SPN(22), Cyst(14), AS(14), SCN(0)
WT 42 (11–67) 2/3 19.9 NA 23(15–68) N(0), SPN(60), Cyst(20), AS(0), SCN(20)
Paiella et al. SVP 54 (23) 25/84 26.1 2 23(23) NA
WT 50 (27) 15/40 26.2 2 30(28) NA
Wang et al. SVP 49.1 ± 7/11 NA NA 29 ± 16 SPN(11.1), N(38.9), SCA(11.1), M(22.2), I(0), Cyst(16.7)
WT 13.6 2/15 NA NA 41 ± 16 SPN(11.8), N(35.3), SCA(17.6), M(23.5), I(5.9), Cyst(5.9)
47.2 ±
15.1
Yohanathan SVP 61(31–84) 9/10 29.9 NA 14(8–65) NA
et al. WT 50 (26–79) 28/35 26.9 NA 24(7–90) NA
Korrel et al. SVP 57(44–67) 234/ 25 1.9 20(13–30) N(45.4), I(13.3), M(8.7), PDAC(3.2), SCN(13.7), O(15.7)
WT 59(44–68) 400 25 2 25 (16–40) N(22.8), I(13.2), M(23.0), PDAC(5.3), SCN(13.2), O(22.5)
79/165
Esposito et al. SVP 50 ± 17 6/18 26 NA 17 ± 10 N(58), M(21), SPN(17), O(4)
WT 41 ± 11 1/9 22 NA 30 ± 21 N(40), M(50), SPN(10), O(0)
Kim et al. SVP 56.3 ± 17/33 24.3 NA 30 ± 20 NA
WT 18.1 4/11 24.3 NA 37 ± 22 NA
54.9 ±
14.5
Lin et al. SVP NA 12/29 NA NA NA SCN(34.1), M(19.5), SPN(12.2), N(14.6), O(19.5)
WT NA 6/5 NA NA NA SCN(27.3), M(18.2), SPN(18.2), N(36.4), O(0)

Ma = male, F = female, BMI = body mass index, ASA = American Society of Anesthesiologists, N=Neuroendocrine tumor, M = Mucinous cystic neoplasm,
I=Intraductal papillary mucinous neoplasm, PDAC=Pancreatic ductal adenocarcinoma, SCN=Serous cystic neoplasm, SPN=Solid pseudopapillary neoplasm,
CN=Cystic neoplasm, SCA=Serous cystadenoma, U=Unknown, AS = Accessory spleen, PC=Pseudocyst, CP=Chronic pancreatitis, MCAC = Mucinous cys­
tadenocarcinoma, AC = Adenocarcinoma, O = other, NA = not available.

analysis. Continuous and categorical variables were calculated as
weighted mean differences (WMDs) or odds ratios (ORs), respectively,
with corresponding 95% confidence intervals (CIs). Heterogeneity was
assessed using the chi-square test, where P < 0.1 was considered sig­
nificant. I2 was used to quantify the statistical heterogeneity, and the
presence of heterogeneity was indicated when I2≥ 50%.
Subgroup analyses were performed by analyzing only high-quality
studies (NOS score ≥7), studies in which operations were performed
via LSPDP and studies with MIDP in which n > 50. The potential
publication bias of the selected studies was assessed using a funnel plot
[23].
3. Results
3.1. Description of trials included in the meta-analysis
A total of 887 relevant studies were initially generated via the search
strategy. These included 347 studies from PubMed, 104 from Embase,

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K. Hang et al.
Fig. 2. Forest plot demonstrating the primary outcome postoperative splenic infarction in terms of SVP-DP versus WT. CI = confidence interval, SVP-DP = splenic
vessels preserving distal pancreatectomy, WT= Warshaw technique.
418 from the Science Citation Index Expanded, and 18 from The
Cochrane Library. To date, no randomized clinical trials have been
conducted. Fig. 1 shows the process of selecting studies using the
PRISMA statement for this meta-analysis. After applying the inclusion/
exclusion criteria, 23 studies with full text were investigated, but one
study [24] overlapped with the most recent study [25], which was
excluded. Another study [26] without detailed data for further synthesis
was excluded, and one study [27] in which both SVP-DP and WT were
performed without comparison was also excluded. Finally, 20 articles
[25,28–46] with full texts were included for detailed analysis and data
extraction. The detailed study characteristics and quality assessments
are listed in Table 1. All the included studies were retrospective cohort
studies. Sixteen studies [25,28,30–34,36–39,41,43–46] were conducted
using MI-SPDP, of which 11 studies [25,28,30,32–34,37–39,41,45]
were related to LSPDP, three [31,44,46] related to RSPDP, and two [36,
43] related to L/RSPDP. Seven studies [25,34,36,38,43,45,46] on
MI-SPDP had sample sizes >50. Fourteen studies [25,29,30,32–34,
36–38,40,42–44,46] with NOS scores ≥7 stars were classified as high
quality.
A total of 2173 patients were included in these studies, of whom
1467 (67.5%) underwent SVP-DP, and 706 (32.5%) underwent WT.
Table 2 shows the baseline and histological characteristics.
3.2. Meta-analysis outcomes
3.2.1. Primary outcome
Eighteen studies [25,28–43,45] reported the primary outcomes of
splenic infarction. A total of 1987 patients were included, of whom 1315
underwent SVP-DP with an incidence of splenic infarction of 4.3% (56 of
1315), and 672 underwent WT with an incidence of 16.7% (112 of 672).
The meta-analysis showed that patients in the SVP-DP group had a lower
rate of splenic infarction than those in the WT group (OR: 0.17; 95% CI,
0.11–0.25; P < 0.00001; Fig. 2). Among 112 patients who developed
splenic infarction in the WT group, less than 10 presented with symp­
toms such as fever, abdominal pain, and/or abscess [25,28].
3.2.2. Secondary outcomes
Compared with the WT group (45/232, 19.4%), the incidence of
gastric varices was significantly lower in the SVP-DP group (24/466,
5.2%), (OR: 0.19; 95% CI, 0.11–0.32; P < 0.00001; Fig. 3A). In the WT
group, none of the patients with gastric varices developed gastrointes­
tinal hemorrhage.
There were no statistically significant differences in the rates of
major complications (OR: 0.98, 95% CI, 0.68–1.41; P = 0.91; Fig. 3B) or
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International Journal of Surgery 103 (2022) 106686
reoperation (OR: 1.05, 95% CI, 0.62–1.78; P = 0.87; Fig. 3C). Pancreatic
tumor size in the SVP-DP group was significantly smaller than that in the
WT group (WMD: 7.27; 95% CI: 9.16 to-5.38; P < 0.00001; Fig. 3D).
The rates of POPF were described in 19 studies [25,28–34,36–46]
(OR: 0.85, 95% CI, 0.65–1.11; P = 0.23), with 2165 patients. Further­
more, as per the ISGPF definition, there was no significant difference in
POPF B/C in 14 studies [25,29–34,36–39,41,43,46] (OR: 0.84, 95% CI,
0.61–1.15; P = 0.28; Fig. 3E) between the SVP-DP and WT groups. There
were no statistically significant differences in blood loss (WMD: 7.15,
95% CI, − 25.27–39.58; P = 0.67; Fig. 3F) or operation time (WMD:
6.02, 95% CI, − 9.41–21.44; P = 0.44; Fig. 3G). Seventeen studies pro­
vided information regarding the length of hospital stay, and the
meta-analysis showed that patients in the SVP-DP group had a shorter
length of hospital stay (WMD: 0.71; 95% CI, − 1.13 to − 0.29; P =
0.0008; Fig. 3H) than those in the WT group.
3.3. Subgroup analyses
The results of the subgroup analyses are summarized in Table 3. The
subgroup analysis, including only high-quality studies, Lap-SPDP, and
MI-SPDP with cases >50, yielded similar results to the primary analysis
except for the length of hospital stay; the subgroup of Lap-SPDP showed
no statistical significance in the duration of the hospital stay (WMD:
0.45; 95% CI, − 1.03 to 0.13; P = 0.13).
3.4. Publication bias
Funnel plots based on splenic infarction are shown in Fig. 4. There
was no evidence of publication bias in splenic infarction.
4. Discussion
Two surgical procedures have been established to preserve the
spleen, SVP-DP and WT, both of which are effective and safe methods for
patients with benign and low-grade malignant neoplasms in the
pancreatic body and tail [43]. SVP-DP was first described by Mallet-Guy
and Vachon [8] in 1943. In 1996, Kimura et al. [12] meliorated and
popularized the method. Owing to its complex anatomic location and
delicate splenic vessels, the SVP-DP needs to preserve the splenic artery
and vein by identifying and ligating numerous small, short vessels that
enter the body or tail of the pancreas. Therefore, it is time-consuming
and challenging to conduct. In 1988, Warshaw [9] reported a new
technique in which the splenic vessels were resected, leaving short
gastric and left gastroepiploic vessels to supply blood to the preserved
K. Hang et al.
Fig. 3. Forest plots demonstrating the secondary outcome in terms of SVP-DP versus WT. (A)Gastric varices; (B) Major complications; (C) Reoperation; (D)
Pancreatic tumor size; (E) Grade B/C postoperative pancreatic fistula; (F) Blood loss; (G) Operation time; (H) Length of hospital stay. SVP-DP = splenic vessels
preserving distal pancreatectomy, WT= Warshaw technique.
spleen. WT has become a valid alternative to SVP-DP. LSPDP was
initially described by Gagner et al. [47] in 1996, and MIDP has gradually
increased in popularity, particularly in recent decades. Several studies
[36,43,46] have successfully applied laparoscopy and robot assistance
for both techniques with an acceptable conversion rate. Inconsistencies
in outcomes between the two techniques still exist, thus, making this
meta-analysis essential.
Previous studies have reported that WT was easier than SVP-DP, and
it was a safe and expeditious procedure that provided a greater likeli­
hood of preserving the spleen [24,48]. However, in our meta-analysis,
more patients underwent SVP-DP (67.5% vs 32.5%), and there was no
statistically significant difference between SVP-DP and WT in terms of
operative time (WMD: 6.02, 95% CI, − 9.14-21.44; P = 0.44) and blood
loss (WMD: 7.15, 95% CI: 25.27–39.58; P = 0.67). The same result was
observed in the LSPDP group. Thus, we suggest that this resulted from
the development of technology and surgeons’ proficiency. In addition,
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International Journal of Surgery 103 (2022) 106686
SVP-DP was related to a shorter length of hospital stay (WMD: 0.71, 95%
CI, − 1.13 to − 0.29; P = 0.0008) as compared to WT, and the relation­
ship was statistically significant.
In our meta-analysis, both overall and detailed complications were
investigated, which would help lead to more specific conclusions. The
incidences of splenic infarction and gastric varices were significantly
higher in the WT group than in the SVP-DP group. This is presumably
due to perfusion defects resulting only from the short gastric and left
gastroepiploic vessels remaining after WT surgery [49]. SVP-DP pro­
cedures preserve the main splenic vasculature, resulting in better
perfusion of the spleen and a reduced risk of infarction and gastric
varices [50]. Although a high incidence of splenic infarction was
observed in the WT group, its relevance was debatable [43] because only
a few patients required a secondary splenectomy; 1.6% of patients (26 of
1621) had splenic infarction (0.6% of SVP-DP vs. 3.6% of WT; OR: 0.23;
95% CI, 0.09–0.57; P = 0.002). Most patients with postoperative splenic
K. Hang et al.
Fig. 3. (continued).
infarction were transient, and no specific treatment was administered.
We presume that the low incidence of secondary splenectomy results
from the better visibility of the splenic vasculature during MIDP in both
groups [43]. Previous studies revealed that the WT was associated with a
higher risk of splenic infarction and gastric varices as compared to the
SVP-DP, as well as a theoretical potential for splenic abscess and
gastrointestinal bleeding [1,51]. However, in our study, less than 10
patients with splenic infarction presented with symptoms, such as fever,
abdominal pain, or abscess, and none of the patients with gastric varices
in the WT group developed gastrointestinal hemorrhage. There was no
statistically significant difference between the SVP-DP and WT groups in
terms of major complications (OR: 0.98; 95% CI, 0.68–1.41; P = 0.91)
and POPF (OR: 0.85; 95% CI, 0.65–1.11; P = 0.23). A previous study
[52], including only grade B/C POPFs, showed that the incidence of
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International Journal of Surgery 103 (2022) 106686
POPF in patients undergoing SVP-DP was significantly lower than that in
WT patients, which contradicts our study. We included the latest studies,
had a larger sample size and found no statistically significant difference
in grade B/C POPF using the ISGPF definition, which could be explained
by the fact that pancreatic stump management remained the same in
both procedures [53].
The pancreatic tumor size in the SVP-DP group was significantly
smaller than that in the WT group, indicating that it is an important
parameter for preoperative decision-making. Dai et al. [38] reported
that a tumor size at a cut-off value of 3 cm was an independent risk factor
for identifying splenic vessels preservation with planned laparoscopic
splenic vessels preservation operations (area under the curve 0.724,
95% CI: 0.63–0.82, P < 0.01). Lin et al. [46] argued that a tumor size at a
cut-off value of 6 cm showed significant differences in the comparison of
K. Hang et al.
Fig. 3. (continued).
RDP with or without splenic preservation, as well as RDP with or
without splenic vessels preservation. Thus, careful assessment of tumor
size is extremely important even before the decision is made. Another
important factor is histopathological diagnosis. Korrel et al. [43] found
that SVP-MIDP was more commonly performed in patients with small
neuroendocrine tumors, suggesting that splenic vessels preservation is
more easily obtained in noninflammatory lesions [54]. Adam et al. [25]
also argued that SVP-DP is technically challenging and may not be
possible if local inflammation is present. Korrel et al. [43] reported that
Warshaw MIDP was more commonly performed in patients with
mucinous cystic neoplasms and larger tumors, suggesting that splenic
vessels preservation is technically more difficult in these types of tu­
mors. There were no statistically significant differences in blood loss
(WMD: 7.15, 95% CI: , − 25.27–39.58; P = 0.67) or operative time
(WMD: 6.02, 95% CI, − 9.41–21.44; P = 0.44) in either group, which
differs from a previous study [55]. We believe this is the result of our
larger sample size, development of technology, and use of more
advanced instruments. Seventeen studies provided information
regarding the length of hospital stay, and the meta-analysis showed that
patients in the SVP-DP group had a shorter length of hospital stay
(WMD: 0.71; 95% CI, − 1.13 to − 0.29; P = 0.0008) as compared to those
in the WT group. A lower incidence of splenic infarction and gastric
varices could explain this difference as it may have a more favorable
impact on the recovery of patients. Our subgroup of Lap-SPDP showed
no statistically significant difference in the duration of the hospital stay
(WMD: 0.45; 95% CI, − 1.03–0.13; P = 0.13), and we concluded that it
was a result of a relatively small sample size.
This study has the following limitations. First, all included studies
were retrospective cohort studies, and almost half had a relatively small
8
International Journal of Surgery 103 (2022) 106686
sample size (<50 patients). Therefore, we conducted a subgroup anal­
ysis to address this issue. Nevertheless, considering the shortcomings of
retrospective studies, a further multicenter randomized controlled study
with a large sample size should be conducted to address this short­
coming. Second, the design of the included studies was unsatisfactory.
Some studies decided on the surgical procedure preoperatively based on
tumor size. Third, we were unable to conduct a subgroup analysis of the
R0/R1 resection rates and long-term survival outcomes of patients with
different histopathological diagnoses, since there were no detailed data
in the included studies. Fourth, the included studies were either from
multiple centers with hundreds of patients or one hospital with several
patients; therefore, the detailed skills differed between different sur­
geons as a result of the influence of the learning curve.
In conclusion, SVP-DP and WT for distal pancreatectomy without
splenectomy are both safe and effective techniques. However, SVP-DP
was associated with less splenic infarction and secondary splenectomy,
although major complications and POPF were comparable. To reduce
postoperative spleen-related complications, SVP-DP should be per­
formed. Finally, tumor size and histopathological diagnosis should be
considered significant parameters before making surgical decisions.
Ethical Approval
Ethical Approval was not required.
Sources of funding
This study was supported by the INTERNATIONAL COOPERATION
Project of Chengdu Science and Technology Bureau (No. 2019-GH02-
K. Hang et al. International Journal of Surgery 103 (2022) 106686

Table 3
Results of subgroup analysis.
Outcome of Interest No. of Studies No. of Patients OR/WMD 95%CI P Heterogeneity I2, %
Value P Value

NOS score≥7
Primary outcome
Splenic infarction 12 1845 0.19 0.12,0.29 ＜0.00001 0.08 39
Secondary outcome
Gastric varices 8 585 0.25 0.08,0.79 0.02 0.02 61
Major complications 8 1760 0.96 0.67,1.39 0.84 0.64 0
POPF 14 2013 0.84 0.63,1.11 0.22 0.81 0
Reoperation 10 1766 1.05 0.62,1.78 0.87 0.95 0
Blood loss 11 1738 14.19 − 25.58,53.96 0.48 ＜0.00001 78
Operation time 12 1781 3.21 − 12.16,18.59 0.68 0.002 62
Length of hospital stay 12 1763 − 0.70 − 1.13,-0.26 0.002 0.12 34
Lap-SPDP
Primary outcome
Splenic infarction 11 674 0.12 0.07,0.21 ＜0.00001 0.95 0
Secondary outcome
Gastric varices 8 475 0.15 0.08,0.29 ＜0.00001 0.12 38
Major complications 5 612 0.77 0.30,1.95 0.58 0.44 0
POPF 11 759 0.75 0.42,1.33 0.32 0.35 11
Reoperation 7 623 1.05 0.35,3.17 0.94 0.92 0
Blood loss 10 734 12.05 − 27.27,51.36 0.55 0.0006 69
Operation time 11 774 2.21 − 17.02,21.44 0.82 ＜0.0001 72
Length of hospital stay 11 756 − 0.45 − 1.03,0.13 0.13 0.25 20
MI-SPDP with cases＞50
Primary outcome
Splenic infarction 6 1454 0.15 0.09,0.25 ＜0.00001 0.61 0
Secondary outcome
Gastric varices 3 362 0.09 0.02,0.39 0.001 0.06 65
Major complications 6 1529 0.96 0.63,1.47 0.87 0.66 0
POPF 7 1581 0.93 0.67,1.30 0.68 0.69 0
Reoperation 4 1375 1.16 0.61,2.20 0.66 0.95 0
Blood loss 7 1596 8.60 − 37.98,55.17 0.72 ＜0.0001 80
Operation time 7 1596 15.26 − 1.18,31.69 0.07 0.001 72
Length of hospital stay 7 1581 − 1.03 − 1.54,-0.52 ＜0.0001 0.14 38

NOS= Newcastle-Ottawa Scale, POPF = postoperative pancreatic fistula, OR = odds ratio, CI = confidence interval.

Research registration Unique Identifying number (UIN)

Name of the registry: International Platform of Registered Systematic

Review and Meta-analysis Protocols database.
Unique Identifying number or registration ID: INPLASY2021120108.
Hyperlink to your specific registration (must be publicly accessible
and will be checked): https://doi.org/10.37766/inplasy2021.12.0108.

Guarantor

Junjie Xiong and Kezhou Li.

6. Provenance and peer review

Not commissioned, externally peer-reviewed.

Data statement
Fig. 4. Funnel plot for publication bias in included studies. splenic infarction.
We are sure our research data available, accessible, discoverable and
useable. All data generated or analyzed during this study are included in
00020-HZ).
this published review article.
Author contribution
Declaration of competing interest
Conception or design of the work: Kuan Hang, Junjie Xiong, Kezhou
The authors declare that they have no known competing financial
Li, Data collection: Lili Zhou, Haoheng Liu, Yang Huang, Analysis and
interests or personal relationships that could have appeared to influence
interpretation of data: Kuan Hang, Lili Zhou, Hao Zhang, Chunlu Tan,
the work reported in this paper.
Drafting the work: Kuan Hang, Lili Zhou, Junjie Xiong, Critical review
and final approval: Kuan Hang, Lili Zhou, Junjie Xiong, Kezhou Li.
Acknowledgements

Disclosure: The authors declare no conflict of interest.

This study was supported by the INTERNATIONAL COOPERATION

9
K. Hang et al.
Project of Chengdu Science and Technology Bureau (No. 2019-GH02-
00020-HZ).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ijsu.2022.106686.
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