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Abstract

Background:

Delayed gastric emptying (DGE) is the most common postoperative complication following any pancreatic resection. The incidence and risk factors of DGE in patients undergoing distal pancreatic resection (DPR) is not well defined. We aimed to determine the incidence of DGE not associated with postoperative pancreatic fistula (POPF) in patients undergoing DPR and to identify predictors of DGE.

Methods:

ACS-NSQIP pancreatectomy database (2014-2017) was queried for patients with pancreatic adenocarcinoma undergoing DPR, excluding patients with POPF. A classification and regression tree (CART) analysis was performed to identify risk for DGE, defined by nasogastric/gastrostomy tube placed after postoperative day (POD) 7 or no oral intake by POD 14.

Results:

A total of 1626 patients underwent DPR without POPF; 59 had DGE (3.6%). Patients with DGE had a longer length of stay vs patients without DGE (median 15 vs 6 days, P < .001). CART analysis showed vascular resection and open surgery were predictors of DGE with a specificity of 98.3%. Patients requiring vascular resection had a 7.8% rate of DGE. Patients who did not undergo open surgery or vascular resection had a 1.8% rate of DGE.

Conclusions:

The rate of DGE in patients undergoing DPR without postoperative pancreatic fistula is low. Predictors of DGE include open surgical approach and vascular resection. These findings may be utilized to counsel patients and take precautions in those at greater risk of developing DGE. Further research can involve implementation of a scoring tool to help stratify patients at risk for DGE after DPR.

Visual Abstract

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Keywords

delayed gastric emptying pancreatic resection risk factors nasogastric tube

Key Learning Points

Delayed gastric emptying can result in increased length of stay and mortality.

Patients with delayed gastric emptying have higher rates of complications.

Vascular resection and open operations are predictors of delayed gastric emptying.

Identifying risk factors for delayed gastric emptying may minimize complications.

Introduction

Delayed gastric emptying (DGE) is the most common postoperative complication following any pancreatic resection.^1,2 DGE has been shown to prolong hospital length of stay and increase hospital costs.^3
-5 Prior to 2007, there was no standardized definition of what constitutes DGE, making it difficult to accurately evaluate the true incidence of this common postoperative complication. To remedy this, the International Study Group of Pancreatic Surgery (ISGPS) proposed a standardized definition of DGE after pancreatic surgery and classified it into three grades. Following the development of this classification system, the incidence of DGE for pancreaticoduodenectomy (PD) has been well established in the literature and ranges from 12% to 60%; however, there is a paucity of data regarding the incidence of DGE for patients undergoing distal pancreatic resection (DPR).

Due to the high rates of DGE after PD, multiple studies have evaluated the risk factors for DGE, which can be categorized as etiologic or complication related. Examples of proposed etiologies for DGE include comorbidities such as obesity and diabetes,^6,7 as well as operative technique.^8
-10 This includes injury of the vagus nerve causing gastric atony, resection of the duodenum causing changes in gastrointestinal hormones, division of gastric arteries or veins leading to ischemia of the stomach, pylorus preservation versus excision, and different techniques for anatomic reconstructions.^11
-13 However, many of these operative related factors are not performed during DPR. In addition, other studies have demonstrated complications such as abscess, hemorrhage, and pancreatic fistula to be associated with DGE.¹⁴ Despite this connection, there is still a substantial incidence of primary DGE, not associated with postoperative pancreatic fistula (POPF) or other post-operative complications.

This study aimed to evaluate the incidence of primary DGE in patients undergoing DPR and identify predictors of DGE in this population.

Methods

This retrospective study utilized the American College of Surgeons-National Surgery Quality Improvement Program (ACS-NSQIP) pancreas targeted database from 2014 to 2017. All patients undergoing DPR for pancreatic adenocarcinoma were identified. Patients with a documented POPF, defined in NSQIP as a drain amylase level three times the normal serum amylase level, were excluded from this study.

The primary outcome was incidence of primary DGE after DPR. DGE is defined in NSQIP by patients requiring a nasogastric tube (NGT) past postoperative day 7 or no oral intake past postoperative day 14. The ACS-NSQIP pancreas database does not grade DGE by the International Study Group of Pancreatic Surgery (ISGPS) definition so there was no differentiation made between ISGPS grades (A, B, and C) of DGE. We compared patients with DGE after DPR to those without DGE after DPR. The secondary aim was to define clinical metrics to classify patients as low and high risk for primary DGE after DPR. Other outcomes measured include demographic variables such as age, gender, and co-morbidities. Operative approach variables were obtained which include planned open, laparoscopic, laparoscopic with unplanned conversion to open, robotic, and robotic with unplanned conversion to open. Operative variables included: vascular resection (artery, vein, vein and artery, not performed), drain placement, number of days after surgery for drain removal, pancreatic duct size, and pancreatic gland texture.

Frequency statistics were performed for all available variables. A Student’s t-test or Mann-Whitney-U test was used to compare continuous variables, and chi-square was used to compare categorical variables for bivariate analysis. Continuous data were reported as medians with interquartile range or as means with standard deviation. Categorical data were reported as percentages.

To study the effects of various factors on the incidence of DGE after DPR we performed a Classification and Regression Trees (CART) method analysis.¹⁵ CART analysis was used to compute a decision tree using the Gini splitting function. In short, this allows for an iterative process where the patient population is divided by outcome according to the variables input by the study authors. CART will output intermediate nodes, as well as terminal nodes which will demonstrate how many patients developed DGE and how many did not. In essence, CART analysis provides a set of significant predictors for a given outcome, in this case being DGE. However, in contrast to classic logistic regression analyses, which aim to provide a complete list of all significant predictors for a set outcome, CART provides the most clinically important variables.^16,17 In order to reduce overfitting while building the tree, pruning in the training data was performed using minimum Cook’s D parameter. The minimum number of parent node cases was 40 while the minimum number of cases for the child nodes was set at 10. The maximum tree depth was set at 4. All analyses were performed with IBM SPSS Statistics for Windows (Version 24, IBM Corp., Armonk, NY).

Results

Demographics, Comorbidities, and Functional Status

A total of 1626 patients who underwent a DPR for pancreatic adenocarcinoma were identified. From this, 59 patients (3.6%) had DGE. Compared to patients without DGE, patients with DGE were of similar age (median, 69 vs 68-years-old, P = .56). When compared to patients without DGE, patients with DGE less commonly had diabetes mellitus (19% vs 31%, P = .042); however, the cohorts were similar in terms of all other comorbidities (all P > .05). In addition, both cohorts were similar in terms of functional status (Table 1).

Table 1.

Demographics of Patients Undergoing Distal Pancreatectomy With and Without Delayed Gastric Emptying.

Characteristic	DGE (n = 59)	No DGE (n = 1567)	P-value
Age, year, median (IQR)	68 (51, 85)	68 (49, 83)	.561
Male, n (%)	29 (49)	834 (53)	.539
Comorbidities, n (%)
Hypertension	30 (51)	901 (58)	.311
Diabetes mellitus	11 (19)	487 (31)	.042
Ascites	0 (0)	2 (0.1)	.784
Bleeding disorder	3 (5.1)	75 (4.8)	.916
COPD	1 (1.7)	88 (5.4)	.194
Smoker	9 (15)	293 (18)	.504
Weight loss	11 (19)	167 (11)	.054
Steroid use	3 (5.1)	48 (3.1)	.382
Congestive heart failure	1 (1.7)	9 (0.6)	.280
Dialysis dependence	0 (0)	8 (0.5)	.582
Ventilator use	0 (0)	1 (0.1)	.846
Functional health status prior to surgery, n (%)
Partially dependent	2 (3.4)	16 (1.0)	.255
Totally dependent	2 (3.4)	18 (1.1)	.125
Preoperative biliary stent, n (%)	0 (0)	18 (1.1)	.503
Chemotherapy within 90 days, n (%)	39 (66)	1161 (74)	.313
Radiation therapy within 90 days, n (%)	49 (83)	1380 (88)	.440

Abbreviations: COPD, chronic obstructive pulmonary disease; DGE, delayed gastric emptying; IQR, interquartile range.

Operative Characteristics and Outcomes

Patients who developed DGE after DPR more commonly had a pancreatic duct size <6 mm (17% vs 8%, P = .035) and had a vascular resection during their surgery (27% vs 12.1%, P = .015). Of the patients who developed DGE after DPR, 7% underwent arterial resection, 15% underwent venous resection, 5% had combined artery/vein resection, and 73% had no vascular resection performed (Table 2). Both cohorts had similar rates of hard, intermediate and soft pancreatic gland texture as well as use of a wound protector. Patients undergoing planned open DPR more commonly developed DGE compared to all other minimally invasive or hybrid surgery techniques (81% vs 62%, P = .002) (Table 2).

Table 2.

Operative Characteristics of Patients Undergoing Distal Pancreatectomy With and Without Delayed Gastric Emptying.

Characteristic	DGE (n = 59)	No DGE (n = 1567)	P-value
Operative approach, n (%)
Open (planned)	48 (81)	969 (62)	.002
Laparoscopic	4 (7)	215 (14)	.430
Laparoscopic – conversion to open	3 (5)	125 (8)	.430
Robotic	1 (2)	96 (6)	.430
Robotic – conversion to open	0 (0)	20 (1)	.430
Pancreatic duct size, n (%)
<3 mm	12 (20)	234 (15)	.035
3-6 mm	10 (17)	132 (8)	.035
>6 mm	0 (0)	49 (3)	.035
Pancreatic gland texture, n (%)
Hard	9 (15)	231 (15)	.130
Intermediate	7 (12)	86 (6)	.130
Soft	17 (29)	389 (25)	.130
Wound protector use, n (%)	25 (42)	677 (43)	.052
Vascular resection, n (%)
Artery	4 (7)	41 (2.6)	.015
Vein	9 (15)	105 (7)	.015
Vein and artery	3 (5)	44 (3)	.015
Not performed	43 (73)	1363 (87)	.015
Drains, n (%)	46 (78)	1340 (86)	.009
Percutaneous drain, n (%)	50 (85)	1498 (96)	<.001
Tumor stage
T1	5 (9)	146 (9)	.302
T2	12 (20)	238 (15)	.302
T3	35 (59)	1085 (69)	.302
T4	5 (9)	43 (3)	.302
Tis	0 (0)	5 (0.3)	.302

Abbreviations: DGE, delayed gastric emptying; MIS, minimally invasive surgery.

When compared to patients without DGE, patients with DGE after DPR had a longer length of stay (median, 15 vs 6 days, P < .001) and a higher rate of readmission (39% vs 12%, P < .001). Patients that developed DGE also had higher rates of 30-day complications including increased transfusions, organ surgical site infections, sepsis, unplanned intubation, ventilator past 48 hours, shock, pneumonia, and myocardial infarction (all P < .001). Patients with DGE after DPR also had increased risk of cardiac arrest with CPR (3% vs 0.5%, P = .005) and increased mortality (3% vs 0.7%, P = .023) when compared to patients without DGE (Table 3). It is also important to note that patients who underwent planned open surgery had an increased mortality rate when compared with patients undergoing a planned minimally invasive approach (1.3% vs 0.3%, P = .025).

Table 3.

Clinical Outcomes in Patients Undergoing Distal Pancreatic Resection With and Without Delayed Gastric Emptying.

Outcome	DGE (n = 59)	No DGE (n = 1567)	P-value
LOS, days, median (IQR)	15 (5, 36)	6 (3, 13)	<.001
Readmission, n (%)	23 (39)	183 (12)	<.001
30-day complications, n (%)
Transfusion	18 (31)	214 (14)	<.001
Organ surgical site infection	10 (17)	74 (5)	<.001
Sepsis	5 (9)	33 (2)	.001
Unplanned intubation	8 (14)	22 (1)	<.001
Ventilator past 48 hours	7 (12)	21 (1)	<.001
Shock	9 (15)	15 (1)	<.001
Pneumonia	7 (12)	37 (2)	<.001
Cardiac arrest with CPR	2 (3)	8 (0.5)	.005
Myocardial infarction	3 (5)	11 (0.7)	<.001
Pulmonary embolism	2 (3)	19 (1)	.146
Mortality, n (%)	2 (3)	11 (0.7)	.023

Abbreviations: CPR, cardiopulmonary resuscitation; LOS, length of stay.

Exploratory CART Analysis in Patients Undergoing DPR

On exploratory CART analysis, vascular resection and open surgery were predictors of DGE with a specificity of 98.3%. Patients requiring vascular resection had a 7.8% rate of DGE while patients without open surgery or vascular resection had a 1.8% rate of DGE. Comorbidities, preoperative chemotherapy/radiation, tumor staging, intraoperative drain placement, hypoalbuminemia or wound protector use were not found to be predictors of DGE (Figure 1).

Figure 1.

Classification and Regression Tree (CART) analysis showing predictors of delayed gastric emptying after distal pancreatectomy.

Discussion

Delayed gastric emptying is associated with significant morbidity and financial cost, with the majority of existing data focusing on outcomes related to pancreaticoduodenectomy. We found the incidence of DGE after DPR for patients not experiencing a POPF to be low, under 4%. In addition, the patients with DGE after DPR had a significantly longer hospital length of stay and an increased rate of mortality. Utilizing a CART analysis, planned open surgery and vascular resection were found to be predictors of DGE with a specificity of over 98%.

The majority of DPR are performed with minimally invasive techniques.^18,19 This national analysis identified planned open DPR to be a predictor of DGE, which in turn is associated with increased length of stay. This is supported by previous prospective, multicenter studies on laparoscopic versus open distal pancreatectomy – for both benign and malignant lesions – which demonstrated prolonged hospital stays for patients with DGE after open DPR.²⁰ In further support, Zhou et al²¹ demonstrated that there was significantly less DGE in the laparoscopic DPR cohort (1.3%) compared to open (28.7%). The underlying mechanism of DGE is poorly understood. Most hypotheses pertain to devascularization or denervation of the pylorus or duodenal resection causing decreased levels of plasma motilin after PD as possible triggers of DGE.²² However, this would not explain the rates of DGE after DPR. Other hypotheses that may pertain to DPR include increased operative time, hormonal changes caused by surgical stress, and postoperative fluid volume status.^23
-25 Minimally invasive technique for DPR may help minimize these risks via less surgical trauma and less perioperative fluid resuscitation.^26
-28

Pancreatic surgery in general has a relatively high rate of requiring major vascular resection. In fact, locally advanced pancreatic cancer with vascular involvement accounts for 30% to 40% of all pancreatic cancer cases.²⁹ Pancreatic body tumors that involved the hepatic or celiac axis were once considered unresectable; however, resections are now being performed with increasing regularity.³⁰ Vascular resection in DPR was found to be a predictor of DGE. This may be related to extensive resections that could affect gastric blood supply and induce DGE.^31
-33 Okada et al³² found that in patients undergoing distal pancreatectomy with celiac axis resection (DP-CAR), resection of the left gastric artery was an independent risk factor for DGE. However, when the left gastric artery was preserved or reconstructed in DP-CAR, there was decreased incidence of DGE.³⁴

Prior to the ISPGS definition, reports on the incidence of DGE after DPR ranged from 0% to 18%.³⁵ More recent reports have stated an incidence of DGE after DPR between 9% and 56.5%, with a high rate of DGE grade A.³⁵ In these studies, the high incidence of DGE after DPR was often associated with a POPF, a known independent risk factor for secondary DGE. Furthermore, there is a lack of large multicenter studies evaluating primary DGE after DPR. However, single center studies by Glowka et al³⁵ and Noorani et al³⁶ identified the rate of DGE in DPR when controlling for pancreatic fistula to be 10% and 12.5% respectively. This current study, which is the largest and only multicenter study looking at primary DGE after DPR, demonstrated a much lower incidence of 3.6%. This may be related to varying definitions of DGE or low sample size in prior studies.

Limitations to this study include those inherent to a retrospective database analysis including misclassification and missing data, documentation of appropriate diagnosis and procedural codes, and reliance on the accuracy of the input of data. Furthermore, the ACS-NSQIP database is limited to data within 30 days of operation and thus does not have long-term outcomes. This database also lacks pertinent clinical information including specific treatments for DGE, the presence and impact of other intra-abdominal processes, multi-visceral resection during index surgery, hospital procedure volume, and surgeon procedure volume, some of which have been demonstrated to be associated with DGE.³⁷ Our study design utilized bivariate comparisons and a CART analysis rather than multivariable regression; therefore, statistical adjustment for covariates is limited, and potential confounding variables cannot be fully excluded – most importantly of which is the impact of planned open surgery versus laparoscopic surgery on outcomes. Despite these limitations, this is the largest, multicenter study looking at the incidence and risk factors for primary DGE in patients undergoing DPR without postoperative pancreatic fistula.

Conclusion

This large, nationwide, multicenter, retrospective database study found the rate of primary DGE in patients undergoing DPR without POPF to be much lower than previously reported. Patients who had DGE after DPR did have increased length of stay and mortality compared to patients without DGE. On CART analysis, vascular resection and open surgery were predictors of DGE after DPR with a specificity of over 98%. These findings may be utilized to counsel patients and take precautions in those at greater risk of developing DGE. Future research utilizing these and other known and novel predictors of DGE may help to develop a clinical scoring tool to stratify patients at risk for DGE after DPR.

Footnotes

ORCID iD

Shray Malik

Ethical Considerations

Ethical approval is not required for this manuscript.

Author Contributions

All authors made a substantial contribution to this work. AG, RW, ZJ, DI, JN, CV, SM, and BS were involved in idea conceptualization, data curation, formal analysis, and writing/review. SM, BS, JN, AG, and ZJ were involved in reviewing and editing of the manuscript.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Use of Artificial Intelligence

No artificial intelligence (AI) was used in the preparation of this manuscript.

References

Dusch

Lietzmann

Barthels

Niedergethmann

Rückert

Wilhelm

TJ.

International study group of pancreatic surgery definitions for postpancreatectomy complications: applicability at a high-volume center. Scand J Surg. 2017;106(3):216-223. doi:10.1177/1457496916680944

Javed

Aziz

Bagante

Wolfgang

CL.

Pancreatic fistula and delayed gastric emptying after pancreatectomy: where do we stand?

Indian J Surg. 2015;77(5):409-425. doi:10.1007/s12262-015-1366-9

Mohammed

GVB

McElhany

Silberfein

Fisher

WE.

Delayed gastric emptying following pancreaticoduodenectomy: incidence, risk factors, and healthcare utilization. World J Gastrointest Surg. 2017;9(3):73. doi:10.4240/wjgs.v9.i3.73

Eisenberg

Rosato

Lavu

Yeo

Winter

JM.

Delayed gastric emptying after pancreaticoduodenectomy: an analysis of risk factors and cost. J Gastrointest Surg. 2015;19(9):1572-1580. doi:10.1007/s11605-015-2865-5

Grossi

Lin

Wong

, et al. Costs and complications: delayed gastric emptying after pancreaticoduodenectomy. Am Surg. 2019;85(12):1423-1428.

Ellis

Gupta

Hewitt

, et al. Risk factors for post-pancreaticoduodenectomy delayed gastric emptying in the absence of pancreatic fistula or intra-abdominal infection. J Surg Oncol. 2019;119(7):925-931. doi:10.1002/jso.25398

Zerbi

Capretti

Commentary to paper “Primary versus secondary delayed gastric emptying (DGE) grades B and C of the International Study Group of Pancreatic Surgery after pancreatoduodenectomy: a retrospective analysis on a group of 132 patients.”

Updat Surg. 2015;67(3):311-312. doi:10.1007/s13304-015-0327-y

Parmar

Sheffield

Vargas

, et al. Factors associated with delayed gastric emptying after pancreaticoduodenectomy. HPB. 2013;15(10):763-772. doi:10.1111/hpb.12129

Bar-Natan

Larson

Stephens

Massey

Delayed gastric emptying after gastric surgery. Am J Surg. 1996;172(1):24-28. doi:10.1016/S0002-9610(96)00048-7

10.

Sun

Zhou

QS.

Clinical risk factors of delayed gastric emptying in patients after pancreaticoduodenectomy: A systematic review and meta-analysis. Eur J Surg Oncol EJSO. 2013;39(3):213-223. doi:10.1016/j.ejso.2012.12.010

11.

Sun

Gou

Zhang

, et al. Complete resection of the gastric antrum decreased incidence and severity of delayed gastric emptying after pancreaticoduodenectomy. Hepatobiliary Pancreat Dis Int. 2021;20(2):182-189. doi:10.1016/j.hbpd.2020.12.001

12.

Kawai

Tani

Hirono

, et al. Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: a prospective, randomized, controlled trial of pylorus-resecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg. 2011;253(3):495-501. doi:10.1097/SLA.0b013e31820d98f1

13.

Shadhu

Ramlagun

Delayed gastric emptying after pancreatic surgery: a review. J Surg. 2018;3(16). doi:10.29011/2575-9760.001177

14.

Courvoisier

Donatini

Faure

Danion

Carretier

Richer

JP.

Primary versus secondary delayed gastric emptying (DGE) grades B and C of the International Study Group of Pancreatic Surgery after pancreatoduodenectomy: a retrospective analysis on a group of 132 patients. Updat Surg. 2015;67(3):305-309. doi:10.1007/s13304-015-0296-1

15.

Breiman

Friedman

Olshen

Stone

CJ.

Classification and Regression Trees. 1st ed. Routledge; 2017. doi:10.1201/9781315139470

16.

Pahl

Sleeper

Canter

, et al. Incidence of and risk factors for sudden cardiac death in children with dilated cardiomyopathy. J Am Coll Cardiol. 2012;59(6):607-615. doi:10.1016/j.jacc.2011.10.878

17.

Mahle

Ohye

, et al. A Predictive model for neurodevelopmental outcome after the Norwood procedure. Pediatr Cardiol. 2013;34(2):327-333. doi:10.1007/s00246-012-0450-1

18.

Partelli

Cinelli

Andreasi

, et al. Evaluation of factors predicting loss of benefit provided by laparoscopic distal pancreatectomy compared to open approach. Updat Surg. 2022;74(1):213-221. doi:10.1007/s13304-021-01194-1

19.

Xourafas

Ashley

Clancy

TE.

Comparison of perioperative outcomes between open, laparoscopic, and robotic distal pancreatectomy: an analysis of 1815 patients from the ACS-NSQIP procedure-targeted pancreatectomy database. J Gastrointest Surg. 2017;21(9):1442-1452. doi:10.1007/s11605-017-3463-5

20.

Yan

Kuang

, et al. Laparoscopic versus open distal pancreatectomy for benign or premalignant pancreatic neoplasms: a two-center comparative study. J Zhejiang Univ-Sci B. 2015;16(7):573-579. doi:10.1631/jzus.B1400257

21.

Zhou

Jin

Wang

, et al. Laparoscopic versus open pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: a propensity score matching analysis. Cancer Commun. 2019;39(1):1-11. doi:10.1186/s40880-019-0410-8

22.

Wente

Bassi

Dervenis

, et al. Delayed gastric emptying (DGE) after pancreatic surgery: A suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142(5):761-768. doi:10.1016/j.surg.2007.05.005

23.

Huang

Han

, et al. Influencing factors of postoperative early delayed gastric emptying after minimally invasive Ivor-Lewis esophagectomy. World J Clin Cases. 2019;7(3):291-299. doi:10.12998/wjcc.v7.i3.291

24.

De Rooij

Van Hilst

Van Santvoort

, et al. Minimally invasive versus open distal pancreatectomy (LEOPARD): a multicenter patient-blinded randomized controlled trial. Ann Surg. 2019;269(1):2-9. doi:10.1097/SLA.0000000000002979

25.

Robinson

Marincola

Shelton

Merchant

Idrees

Parikh

AA.

Peri-operative risk factors for delayed gastric emptying after a pancreaticoduodenectomy. HPB. 2015;17(6):495-501. doi:10.1111/hpb.12385

26.

Han

Seo

Koo

Lee

. Comparison of intraoperative basal fluid requirements in distal pancreatectomy: laparotomy vs. laparoscopy a retrospective cohort study. Medicine (Baltimore). 2017;96(47):e8763. doi:10.1097/MD.0000000000008763

27.

Xie

Zhu

Chen

Yan

Mou

YP.

Laparoscopic distal pancreatectomy is as safe and feasible as open procedure: a meta-analysis. World J Gastroenterol. 2012;18(16):1959. doi:10.3748/wjg.v18.i16.1959

28.

Abu Hilal

Hamdan

Di Fabio

Pearce

Johnson

CD.

Laparoscopic versus open distal pancreatectomy: a clinical and cost-effectiveness study. Surg Endosc. 2012;26(6):1670-1674. doi:10.1007/s00464-011-2090-6

29.

Van Veldhuisen

Van Den Oord

Brada

, et al. Locally advanced pancreatic cancer: work-up, staging, and local intervention strategies. Cancers. 2019;11(7):976. doi:10.3390/cancers11070976

30.

Klompmaker

Peters

Van Hilst

, et al. Outcomes and risk score for distal pancreatectomy with celiac axis resection (DP-CAR): an international multicenter analysis. Ann Surg Oncol. 2019;26(3):772-781. doi:10.1245/s10434-018-07101-0

31.

Kondo

Katoh

Hirano

, et al. Ischemic Gastropathy after distal pancreatectomy with celiac axis resection. Surg Today. 2004;34(4):337-340. doi:10.1007/s00595-003-2707-z

32.

Okada

Kawai

Tani

, et al. Preservation of the left gastric artery on the basis of anatomical features in patients undergoing distal pancreatectomy with celiac axis En-Bloc resection (DP-CAR). World J Surg. 2014;38(11):2980-2985. doi:10.1007/s00268-014-2702-0

33.

Yamamoto

Sakamoto

Ban

, et al. Is celiac axis resection justified for T4 pancreatic body cancer? Surgery. 2012;151(1):61-69. doi:10.1016/j.surg.2011.06.030

34.

Sato

Saiura

Inoue

Takahashi

Arita

Takemura

Distal pancreatectomy with En Bloc resection of the celiac axis with preservation or reconstruction of the left gastric artery in patients with pancreatic body cancer. World J Surg. 2016;40(9):2245-2253. doi:10.1007/s00268-016-3550-x

35.

Glowka

Von Websky

Pantelis

, et al. Risk factors for delayed gastric emptying following distal pancreatectomy. Langenbecks Arch Surg. 2016;401(2):161-167. doi:10.1007/s00423-016-1374-7

36.

Noorani

Rangelova

Del Chiaro

Lundell

Ansorge

Delayed gastric emptying after pancreatic surgery: analysis of factors determinant for the short-term outcome. Front Surg. 2016;3. doi:10.3389/fsurg.2016.00025

37.

Lytras

Paraskevas

Avgerinos

, et al. Therapeutic strategies for the management of delayed gastric emptying after pancreatic resection. Langenbecks Arch Surg. 2007;392(1):1-12. doi:10.1007/s00423-006-0096-7