Risk Factors for Reoperation After Debridement of Acute Pancreatitis

j o u r n a l o f s u r g i c a l r e s e a r c h  j u l y 2 0 2 0 ( 2 5 1 ) 6 3 e7 0

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Risk Factors for Reoperation After Debridement of Acute Pancreatitis Zhao Zhifeng, MD,a,b Xie Rongli, MD,b Li Li, MD,a Zhang Jun, PhD,b Shen Dongjie, MD,c Xu Zhiwei, MD,b,** Mao Enqiang, PhD,d and Fei Jian, PhDb,* a

School of Clinical Medicine, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine, Shanghai, China b Department of General Surgery, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine, Shanghai, China c Department of General Surgery, Luwan Branch, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine, Shanghai, China d Department of Emergency, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine, Shanghai, China

article info

abstract

Article history:

Background: Acute pancreatitis (AP) is a common gastrointestinal disorder with a high

Received 22 May 2018

mortality rate. This study evaluated the incidence of and risk factors for reoperation after

Received in revised form

debridement of AP.

31 October 2019

Methods: This retrospective study included 168 patients diagnosed with AP who had un-

Accepted 18 November 2019

dergone debridement between January 2007 and December 2017 at our hospital. Patients

Available online xxx

were divided into single-operation and reoperation groups separately. Results: Sixty-eight (40.24%) patients underwent reoperation after AP debridement. The

Keywords:

main procedure for reoperation was debridement of necrosis. In univariate analysis, the

Acute pancreatitis

risk factors for reoperation included younger age; higher admission temperature and heart

Surgery

rate; higher levels of C-reactive protein (CRP), blood urea nitrogen and creatinine; higher

Debridement

Acute Physiology and Chronic Health Evaluation II score and rate of continuous renal

Surgical indication

replacement therapy; shorter operation interval; lower postoperative albumin level; and

Reoperation

high incidence of preoperative and postoperative complications. Multivariate logistic analysis indicated that independent risk factors for reoperation included higher levels of Creactive protein and creatinine in admission, preoperative percutaneous catheter drainage, and postoperative complications. Conclusions: The general characteristics and clinical procedures of patients with AP after debridement might affect prognosis and reoperation. The identification of risk factors could help clinicians to provide specific treatment, better ward management, and stratification of reoperation risk. ª 2019 Elsevier Inc. All rights reserved.

Permanent address: Pancreatic treatment center, Ruijin Hospital, No. 197, Ruijin No.2 Road, Huangpu District, Shanghai * Corresponding author. Department of General Surgery, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine, No. 197, Ruijin No.2 Road, Huangpu District, Shanghai, China. Tel.: þ86 189 1670 3777; fax: þ86-021-64370045. ** Corresponding author. Department of General Surgery, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, School of Medicine, No. 197, Ruijin No.2 Road, Huangpu District, Shanghai, China. Tel.: þ86 189 1776 2956; fax: þ86-021-64370045. E-mail addresses: [email protected] (X. Zhiwei), [email protected] (F. Jian). 0022-4804/$ e see front matter ª 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jss.2019.11.023

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Introduction Acute pancreatitis (AP) is the third most common gastrointestinal disorder in the United States. AP is associated with rapid progression, various complications, poor prognosis, and high mortality and has become one of the most costly diseases, exceeding $2 billion annually.1,2 The pathogenesis of AP involves activation of pancreatic enzymes and secondary inflammatory responses that are usually associated with infection of pancreatic or peripancreatic necrotic tissue or even multiple organ failure (MOF) and sepsis. Surgical intervention is required for patients with infected pancreatic necrosis (IPN), MOF, and abdominal compartment syndrome (ACS). Nowadays, the major interventional therapy for AP is the minimally invasive step-up approach in which patients with limited lesions are managed by surgical treatment such as percutaneous catheter drainage (PCD). If the patients do not respond to this treatment, or in more complex cases, open surgery is needed.3,4 The main method of laparotomy is debridement with continuous peritoneal lavage. Because of the acute inflammation, severe infection, and huge surgical trauma, debridement of AP is usually associated with a variety of complications that need unplanned reintervention. Pancreatic debridement is frequently accompanied with morbidity of 34%-95% and mortality of 11%-39%.5,6 Early postoperative complications include hemorrhage, local infection, intestinal fistula, and pancreatic fistula, and late complications include exocrine pancreatic insufficiency and diabetes. Among them, hemorrhage, fistula, and secondary infection often require reintervention. It is suggested that 60%-70% of patients undergo reoperation after the first pancreatic debridement.7,8 The incidence of intestinal fistula, hemorrhage, and pancreatic fistula in the reoperation patients can reach as high as 80%, which results in worse prognosis and survival.9 Therefore, it is important to identify the risk factors for reoperation. By dividing patients by gradient risk stratification, surgeons can provide individualized treatment for different patients. In the present study, 176 patients at our center who had undergone pancreatic debridement in the past 10 y were analyzed for incidence of and risk factors for reoperation.

accordance with the revised Atlanta criteria10; (3) patients who had undergone at least one debridement of AP necrosis in our hospital; and (4) reoperation must have been secondary debridement or hemostasis caused by pancreatic or peripancreatic infection or bleeding during the perioperative period of the first pancreatic debridement. Exclusion criteria included traumatic pancreatitis, combined with other benign or malignant pancreatic tumors, and those who died during the perioperative period after the first debridement. In accordance with these criteria, we enrolled 176 patients. All patients received the same standard treatment including fluid therapy, gastrointestinal decompression, pain control, nutritional support, anti-infection, and inhibition of pancreatic secretion.11,12 The antibiotics strategy was prophylactic antibiotics at administration and adjusted by corresponding purulent fluid culture and drug sensitivity. Minimally invasive approaches were conducted first if necessary. Hemofiltration was used to treat patients with combined renal insufficiency. For patients with massive hemorrhage, digital subtraction angiography or subsequent transcatheter arterial embolization was performed first. Laparotomy was used when nonoperative therapy was unable to control disease progression. All the operations were decided by the multidisciplinary team, which consisted of departments of imaging, intensive care unit (ICU), and anesthesiology, to ensure the surgical indications. The operation was usually performed through a subcostal or a midline longitudinal incision. In general, blunt dissection was used for debridement to avoid complete resection and reduce the risk of bleeding and pancreatic fistula. Cholecystectomy could also be performed to prevent probable biliary pancreatitis in the future.13

Data collection Patient data were collected from our hospital database. The variables chosen were demographics, etiology, vital signs, laboratory examination, imaging examination, approach of intervention, complications, and outcomes. The Acute Physiology and Chronic Health Evaluation (APACHE) II score was also calculated.

Methods

Definitions

This retrospective study was conducted at our hospital and included all the patients with acute pancreatitis who received debridement between January 2007 and November 2017. All the procedures were implemented based on the principles of the Declaration of Helsinki, and the design of the work was reviewed and approved by the ethics committee of our hospital. As this is a retrospective research, patient consent was waived by our institutional ethics committee.

The IPN is diagnosed by purulent culture in celiotomy. Hemorrhage was defined as the reduction of >2 g/dL and/or significant hemodynamic deterioration caused by intraperitoneal hemorrhage.14 Shock was defined as systolic pressure <90 mmHg or a requirement for positive inotropic drugs. Respiratory failure was defined as the ratio of arterial oxygen pressure and inspired oxygen concentration (PaO2/FiO2) 300 mmHg. Liver failure was defined as the Marshall score 2. Renal failure was defined as serum creatinine >176 mmol/L (2 mg/dL). ACS was defined as persistent intra-abdominal pressure >20 mmHg with new organ dysfunction.15 Other complications were defined in accordance with the Atlanta classification of AP.10 The continuous variables were transformed into dichotomized in logistic regression, and their normal range were as follows: heart rate (HR) < 100 bpm, C-

Patients Inclusion criteria (1) included the following: all patients who were diagnosed with AP at our hospital between January 2007 and November 2017; (2) diagnostic criteria of AP defined in

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zhifeng et al  reoperation risk factors of acute pancreatitis debridement

Table 1 e Baseline characteristics of patients undergoing debridement of acute pancreatitis. Variable Age, y

Single-operation group (n ¼ 101)

Reoperation group (n ¼ 68)

P value

51.30  13.21

46.76  15.45

0.043

0.635

Sex, no. (%) Female

34 (33.3)

20 (29.9)

Male

68 (66.7)

47 (70.1)

24.15  3.04

24.42  4.21

0.730

0.502

BMI, kg/m2 Etiology, no. (%) Gallstones

54 (52.9)

29 (43.3)

HTG

16 (15.7)

18 (26.9)

Alcohol

7 (6.9)

4 (6.0)

Post-ERCP

5 (4.9)

3 (4.5)

20 (19.6)

13 (19.4)

Smoke

22 (25.6)

12 (18.2)

0.278

Alcohol

24 (27.9)

15 (22.7)

0.469

Hypertension

23 (26.7)

19 (28.8)

0.780

6 (7.0)

10 (15.2)

0.104

Others Comorbidities, no. (%)

DM CAD

3 (3.5)

2 (3.0)

0.875

FLD

4 (4.7)

2 (3.0)

0.611

SD ¼ standard deviation; BMI ¼ body mass index; HTG ¼ hypertriglyceridemia; ERCP ¼ endoscopic retrograde cholangiopancreatography; DM ¼ diabetes mellitus; CAD ¼ coronary artery disease; FLD ¼ fatty liver disease.

reactive protein (CRP) <100 mg/L, blood urea nitrogen (BUN) <7.5 mmol/L, creatinine <115 mmol/L, and albumin >35 g/L.

Statistical analysis All of the analysis was performed using SPSS for Windows, version 22.0 (IBM Analytics, Armonk, NY). Data were analyzed using mean, standard deviation, and Student’s t-

test for continuous variables. As for categorical variables, frequency and Pearson’s c2 test were conducted if required. The risk factors for reoperation after debridement of AP were determined using two-step logistic regression. The first step was univariate regression to assess the association between reoperation and risk factors. The second step was binary stepwise logistic regression using a forward selection method.

Table 2 e Comparison between single-operation and reoperation groups at admission. Single-operation group (n ¼ 101)

Reoperation group (n ¼ 68)

Temperature,  C

37.51  0.66

37.77  0.86

MAP, mmHg

96.16  14.29

95.41  13.64

0.744

HR, bpm

101.33  20.77

114.86  21.81

<0.001

RR, bpm

23.08  5.82

24.71  6.75

0.117

109.30  27.30

104.37  29.22

0.311

28.71  5.68

27.78  5.70

0.344

Variable

P Value

Vital signs 0.043

Examination Hemoglobin, g/L Albumin, g/L 9

227.18  108.90

192.90  120.37

0.087

CRP, mg/L

92.99  72.06

129.28  74.12

0.022

TB, mmol/L

36.83  52.90

52.49  70.81

0.141

6.37  4.33

13.64  10.27

<0.001

82.91  79.38

193.13  191.69

<0.001

12.57  6.55

18.80  8.66

<0.001

Platelet, x10 cells/L

BUN, mmol/L Creatinine, mmol/L Score APACHE II

MAP ¼ mean arterial pressure; HR ¼ heart rate; RR ¼ respiratory rate; CRP ¼ C-reactive protein; TB ¼ total bilirubin; BUN ¼ blood urea nitrogen; APACHE II ¼ Acute Physiology and Chronic Health Evaluation II.

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Table 3 e Clinical procedures, complications, and outcomes between single-operation and reoperation groups. Variable

Single-operation group (n ¼ 101)

Reoperation group (n ¼ 68)

50 (49.0)

25 (37.3)

P value

Procedure PCD, no. (%) CRRT, no. (%)

7 (9.7)

25 (41)

0.134 <0.001

Interval, no. (%)

54.85  49.47

35.79  36.44

0.007

Post Alb, g/L

31.44  4.57

28.33  4.78

<0.001

23 (22.8)

21 (31.3)

0.216

ED

9 (8.9)

25 (37.3)

<0.001

RF

19 (18.8)

34 (50.7)

<0.001

8 (7.9)

16 (23.9)

0.004

10 (9.9)

17 (25.4)

0.008

ACS

3 (3.0)

8 (11.9)

0.021

ARF

13 (12.9)

23 (34.3)

0.001

Complications before operation Sepsis

Hemorrhage Shock

Complications after operation ACS

0 (0.0)

5 (7.5)

0.005

IPN

35 (34.7)

58 (86.6)

<0.001

Sepsis

14 (13.9)

24 (35.8)

0.001

MOF

4 (4.0)

16 (23.9)

<0.001

ARF

8 (7.9)

29 (43.3)

<0.001

10 (9.9)

33 (49.3)

<0.001

Shock

6 (5.9)

34 (50.7)

<0.001

Intestinal fistula

3 (2.9)

25 (37.3)

<0.001

Hemorrhage

6 (5.9)

32 (47.8)

<0.001

RF

Outcome Third operation Mortality ICU durations

/

55 (80.9)

/

4 (4.1)

11 (16.7)

0.006

32.97  41.62

80.43  90.46

<0.001

PCD ¼ percutaneous catheter drainage; CRRT ¼ continuous renal replacement therapy; Interval ¼ the interval between onset and first debridement; post Alb ¼ postoperative albumin at 24 h; ED ¼ electrolyte disturbance; RF ¼ respiratory failure; ACS ¼ abdominal compartment syndrome; ARF ¼ acute renal failure; IPN ¼ infected pancreatic necrosis; MOF ¼ multiple organ failure; ICU ¼ intensive care unit.

Results One hundred one patients were cured by a single operation, and the other 68 underwent multiple operations. The age of the patients who were cured by a single operation was significantly higher than that of the reoperation group (P ¼ 0.043). There were no significant differences in other variables including gender, body mass index, etiology, and morbidity. The etiological factors consisted of gallstones, hypertriglyceridemia, alcohol, postoperative endoscopic retrograde cholangiopancreatography, and others. The main comorbidities included smoking, alcohol, hypertension, diabetes mellitus, coronary heart disease, and fatty liver disease (Table 1). In admission characteristics, the temperature, HR, CRP, BUN, creatinine, and APACHE II scores in the reoperation group were significantly higher than those in the singleoperation group, suggesting a greater risk of reoperation in those with worse general health. Besides, there were no significant differences in mean arterial pressure, respiratory rate, hemoglobin, albumin, platelets, and total bilirubin between the two groups (Table 2).

In accordance with our data, the incidence of common postoperative complications was as follows: local complications included secondary infection (55.0%), hemorrhage (22.5%), intestinal fistula (16.6%), and abdominal hypertension (3.0%). Systemic complications included respiratory failure (25.4%), shock (23.7%), sepsis (22.5%), acute renal failure (21.9%), and MOF (11.8%). There were many variables that differed significantly during treatment. Patients in the reoperation group had a higher rate of continuous renal replacement therapy (CRRT), shorter operative intervals, lower postoperative albumin, higher incidence of preoperative complications including electrolyte disorders, respiratory failure, bleeding, shock, ACS and acute renal failure, and higher incidence of postoperative complications including ACS, IPN, sepsis, MOF, acute renal failure, respiratory failure, shock, intestinal fistula, and hemorrhage. At the same time, the mortality was higher and intensive care unit (ICU) duration was significantly longer in the reoperation group. There were no differences in the rate of PCD and sepsis between the groups. In addition, 80.9% of reoperation patients underwent three or more operations, which suggested the complexity of AP (Table 3). The results of univariate logistic

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zhifeng et al  reoperation risk factors of acute pancreatitis debridement

Table 4 e Univariate logistic regression of reoperation after debridement of acute pancreatitis. Variable

Odds ratio

95% CI

P Value

Age <50

Reference

Reference

Reference

40-50

5.000

0.953

16.767

Reference 0.057

50-60

1.667

0.300

9.272

0.560

60-70

2.609

0.486

14.004

0.263

>70

2.462

0.463

13.076

0.290

Sex Male

Reference

Reference

Reference

Female

0.921

0.475

1.784

Reference 0.807

Smoke

0.646

0.293

1.426

0.280

Alcohol

0.760

0.361

1.599

0.469

BMI <18.5 18.5-24.9

6.353

0.654

61.725

Reference

Reference

Reference

0.111 Reference

25-29.9

2.118

0.421

10.650

0.363

>30

1.271

0.519

3.108

0.600

Etiology

0.354

Gallstones

Reference

Reference

Reference

HTG

1.988

0.885

4.462

Reference 0.096

Alcohol

1.010

0.273

3.732

0.989

Post-ERCP

1.060

0.237

4.749

0.939

Others

1.148

0.501

2.632

0.744

HR

1.740

1.268

2.388

0.001

CRP

1.475

1.059

2.053

0.021

BUN

2.511

1.714

3.680

<0.001

Creatinine

2.304

1.594

3.329

<0.001 <0.001

APACHE II

2.446

1.546

3.868

PCD

0.619

0.330

1.161

0.135

Interval

0.578

0.433

0.773

<0.001

Post Alb

0.493

0.323

0.752

0.001

Precomplication

5.814

2.673

12.645

<0.001

Postcomplication

26.526

8.942

78.692

<0.001

post Alb ¼ postoperative albumin at 24 h; Interval ¼ the interval between onset and first debridement.

regression about the risk factors were presented in Table 4. Furthermore, multivariate logistic regression suggested that higher CRP and creatinine at admission, lower preoperative PCD rate, and higher incidence of postoperative complications were independent risk factors of reoperation after debridement of AP (Table 5). The most common surgical procedure after the first debridement of AP included debridement (70.59%) and

Table 5 e Multivariate logistic regression of reoperation after debridement of acute pancreatitis. Variable CRP

Odds ratio 2.359

95% CI 1.255

4.436

P Value 0.008

Creatinine

2.826

1.224

6.524

0.015

PCD

0.164

0.033

0.805

0.026

59.725

4.589

777.231

0.002

Postcomplications

Interval = the interval between onset and first debridement.

hemostasis (29.41%). Patients with alcohol abuse, higher HR at admission, and higher incidence of preoperative complications were more prone to be treated with hemostasis after the first debridement. No other significant differences were found between the groups (Table 6).

Discussion AP is a disease with acute onset and poor prognosis. In severe cases, the mortality can even reach 20%-30%.16 For those who were diagnosed with IPN, MOF, or ACS, surgery is indispensable. However, after surgical debridement, some patients might have recurrent infection or hemorrhage that requires reoperation. Therefore, we analyzed the risk factors for reoperation in 169 cases of AP at our hospital. We retrospectively studied 169 patients with AP after debridement between January 2007 and December 2017; of whom, 68 underwent reoperation. The mortality rate was

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Table 6 e Comparison between different procedures of the second operation after debridement of AP. Debridement (n ¼ 48)

Hemostasis (n ¼ 20)

48.77  14.52

41.10  16.70

Male

27 (56.3)

20 (100.0)

Female

21 (43.8)

0 (0.0)

Smoke

7 (15.2)

5 (25.0)

0.344

Alcohol

7 (15.2)

8 (40.0)

0.027

24.17  4.25

25.00  4.25

0.572

Gallstones

24 (50.0)

6 (30.0)

HTG

12 (25.0)

6 (30.0)

2 (4.2)

2 (10.0)

Variable Age

P value 0.062

Sex

BMI Etiology

Alcohol

<0.001

0.374

Post-ERCP

1 (2.1)

2 (10.0)

Others

9 (18.8)

4 (20.0)

HR

110.93  19.73

123.90  24.14

CRP

123.88  75.18

137.76  74.39

0.591

BUN

12.42  9.75

16.08  11.09

0.195

Creatinine

150.00  125.16

279.4  264.95

0.050

APACHE II

19.00  9.25

18.40  7.54

0.803

PCD

0.025

18 (37.5)

7 (35.0)

0.846

Interval

38.02  42.26

29.00  13.30

0.189

Post Alb

28.39  5.11

28.20  4.21

0.884

Precomplication

38 (79.2)

20 (100.0)

0.027

Postcomplication

44 (91.7)

20 (100.0)

0.183

Third operation

38 (79.2)

17 (85.0)

0.577

7 (14.9)

4 (20.0)

0.606

Mortality post Alb ¼ postoperative albumin at 24 h.

16.7% in the reoperation group and 4.1% in the singleoperation group. The ICU duration was 80.4 d in the reoperation group and 33.0 d in the single-operation group, indicating that the patients suffered more in the reoperation than in the single-operation group. For the second operation, exploratory debridement accounted for 70.6% of cases, which was consistent with the prior study.17 Early-stage treatment of AP was mainly fluid resuscitation, and surgical intervention was used unless conservative treatment was ineffective. The main surgical protocol is a step-up approach that comprises PCD, endoscopic drainage, and endoscopic and open debridement.18-20 It is reported that preoperative PCD can reduce the mortality in patients with IPN from 40% to 18%,21 and it can relieve the condition in 62.5% of patients with sepsis and 36.6% of those with MOF.22 The surgical treatment was performed when minimally invasive surgery is not possible. The standard operating procedure includes debridement of pancreatic necrosis and continuous postoperative lavage.23 Recent studies suggest that surgery beyond 28-30 d after onset can effectively reduce the incidence of postoperative morbidity and mortality.24 As the parcel boundary formed between the necrotic tissue and normal tissue in this period, the operation could remove the necrotic tissue completely and reduce the risk of postoperative hemorrhage and sepsis.25 In accordance with our results, the average timing for the

single-operation group was up to 53 d after onset of AP, and the reoperation group was 35 d after onset of AP. Both had been delayed for up to 4 wk. Multivariate analysis suggested that there was no significant difference between the two groups, which means the additional increasement of surgical timing for more than 30 d could not reduce the risk of reoperation. In univariate analysis, the significant risk factors included age, admission temperature, admission HR, CRP, BUN, creatinine, APACHE II score, CRRT, surgical timing, postoperative albumin, and preoperative and postoperative complications except for preoperative sepsis. In subsequent multivariate analysis, the independent risk factors for reoperation included admission CRP and creatinine, preoperative PCD, and postoperative complications. Based on previous studies, admission CRP and creatinine were the most important biochemical indicators of the severity of AP.26-29 The abnormal elevation of CRP and creatinine levels at admission indicated severe illness and poor general condition, which may increase the risk of reoperation. PCD reduces absorption of endotoxin through drainage and relieves the systemic inflammatory responses, which is conducive to postoperative recovery and decreases the risk of reoperation. The occurrence of postoperative complications is associated with poor recovery, which usually means an increased risk of reoperation.

zhifeng et al  reoperation risk factors of acute pancreatitis debridement

Among the variants, we found it interesting that the age of reoperation groups is lower than that in the single-operation group. There are some possible explanations. First, serious infectious pancreatic necrosis which requires surgical intervention was generally more common in younger patients. Second, older patients were more likely to lose the chance of surgery because of the worse physical condition. Third, although the average age was markedly lower in the reoperation group, there was still no significant difference in multivariant logistic analysis. It might be necessary to expand cases for further verification. Unplanned reoperations increase the cost of health care significantly, which includes the expenses, suffering and mortality of patients, the turnover rate and efficiency of the hospital, and allocation of medical resources. The risk factors of reoperation after pancreatic resection has been studied,30 which suggests that its rate of reoperation was 5.0% and several patient characteristics and procedural factors could influence it. However, no studies have been carried out on reoperation for AP. Considering its complexity, the reoperation and multiple operations are common in patients with AP, which incurs high medical costs. Hence, it is important to investigate the risk factors for reoperation after debridement of AP. This is believed to be the first study to explore the risk factors for reoperation for AP. Our study confirmed several possible risk factors. For clinicians, it is necessary to pay more attention to possible risk factors and handle those issues timeously. For ward management, Enhanced Recovery after Surgery protocols could be used in the supervision of high-risk patients and improve overall. For the development of related guidelines, patients with AP after debridement could be stratified based on risk so as to improve the overall medical efficiency. There were several limitations to our study. A retrospective study was conducted to estimate the risk factors for reoperation in the past 10 y, which may have resulted in selection bias. In addition, only 169 patients were investigated, and multicenter studies are needed in the future with more patients. In conclusion, the independent risk factors for reoperation for patients with AP included CRP, creatinine at admission, preoperative PCD, and postoperative complications. The main procedure for reoperation was debridement of necrosis. The identification of risk factors could help clinicians to provide specific treatment, better ward management, and stratification of reoperation risk. The final purpose is to reduce the number of unplanned reoperations and improve the treatment efficacy and survival of patients.

Acknowledgment The authors would like to thank Jingyi Wu, Jianhua Gu, Erzhen Chen. Jun Zhang and Dongjie Shen made substantial contributions to the manuscript and the analysis of data. Rongli Xie and Li Li participated in the data collection. Zhiwei Xu, Enqiang Mao, and Jian Fei participated in drafting or revising the work. Zhifeng Zhao was responsible for the organization

69

of the group and drafted the manuscript. All authors have given final approval of the version to be published. All authors agreed to be accountable for all aspects of the manuscript. This study is financially supported by the National Natural Science Fund of China (Project No. 81670581 to Jian FEI).

Disclosure The authors reported no proprietary or commercial interest in any product mentioned or concept discussed in this article.

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