Introduction

The pancreaticoduodenectomy(PD)is a standard procedure used to resect lesions in the periampullary area,including benign and malignant diseases.It is also a complex and difficult surgical procedure,involving multiple organ resections and lymph node dissection [1,2].Abdominal infection,postoperative pancreatic fistula(POPF),and intra-abdominal hemorrhage are common complications after the procedure.Mortality related to PD is mostly caused by hemorrhage.The mortality rate has recently decreased from 25–30%to less than 5%in some surgical centers[3,4].Despite the dramatic decrease in the mortality rate,its morbidity rate after PD remains relatively high.POPF is thought to be associated with all of these postoperative complications and can cause an overall increase in both the morbidity and mortality[5].

We introduced a suspender pancreaticojejunostomy(PJ)method to replace the traditional end-to-side invagination PJ[6,7].The suspender PJ shortens the procedure in a more reliable manner.Most important,it signi ficantly reduces the incidence of POPF compared to the traditional end-to-side invagination PJ.The present study analyzed the correlation between the risk factors and the incidence of POPFs in patients who underwent the PD,and compared the incidence of POPF between patients subjected to traditional end-to-side invagination PJ and those to suspender PJ.

目前的研究皆证实了修正性反馈对英语冠词习得的促进作用，但实验的范围仅限于对简单冠词用法的反馈（首次提及和再次提及的用法），至于修正性反馈是否对复杂冠词用法有效还有待探讨。

Methods

Patients

Data of 335 patients who underwent the PD from January 2006 to January 2014 were involved in the prospective database.All eligible participants who received surgical operations from the same surgeon team in our hospital were histologically diagnosed to have periampullary lesions,including distal bile duct carcinoma,duodenal papillary carcinoma,carcinoma of pancreas head,ampullary carcinoma,ampullary benign diseases,and some other rare malignancies.Of these patients,147 received the traditional end-to-side invagination PJ and 188 the suspender PJ.Patient eligibility was determined based on the inclusion and exclusion criteria as follows.Inclusion criteria:(i)patients with resectable lesions in the periampullary area,who were con firmed by pathological diagnosis,including benign and malignant diseases;(ii)patients with available informed consent or waiver of consent;and(iii)patients with available follow-up information.Exclusion criteria:(i)patients missing informed consent;and(ii)patients with unresectable tumor in the periampullary area or tumor distant metastasis.

对我们来说，我们的工作除了要将优秀的设计提供给像酒店、地产商这样专业的客户，我们更要尝试把优秀的设计带进更多人的生活中去。以我自己的WS SPACE 無·集为例。这里是一个能够用设计感染人的空间。在这里设计和人们之间几乎没有距离，在这里你可能喝完一杯咖啡就发现眼前的杯子能给你此时此刻带来一丝愉悦，这其实就是所谓的设计走进生活。同理，你在这里闻到某个香薰时，它也会给你带来片刻的联想以及所谓的氛围营造。我个人很喜欢用这些小的东西去影响、感染别人，而我设计这个空间的目的就在于将设计与美的东西带给更多人。

Fig.1.The procedure of suspender PJ.A:First,cut off the neck of pancreas.Second,found out the pancreatic duct and insert the drainage tube(blue arrow),and then fixed the tube on the glands around it by 3–0 absorbable suture.Last,suture the pancreatic section by nylon threads to stop bleeding(yellow arrow).B:An incision shorter than diameter of the pancreatic stump was made in the intestinal wall opposite to the jejunal mesentery,and then 3–0 proline was used to perform purse-string suture along the incision in the intestinal wall.C and D:Another small hole was made 3–4 cm away from the incision of the jejunum,and the drainage tube of pancreatic duct was pulled out of the hole.After that,the stump of the pancreas was enveloped into the jejunal incision by pulling the nylon threads sutured in the pancreatic section.E:Relaxation suture was performed using two or three stiches between jejuna seromuscularis and capsule of the pancreas(blue arrow).F:3–0 proline purse-string suture is tightened(yellow arrow)and the suspender PJ finished.G:To check if there was any leakage of pancreatic intestinal anastomosis by water injection.H:Cut off the nylon threads along the jejunal wall,and closed the hole in the jejunum wall where the drainage tube out of by purse string suture.

Surgical procedure

In this study,the univariate analysis showed that the pancreatic texture,PJ method,postoperative abdominal infection,and abdominal bleeding were associated with POPF.The soft pancreas texture was a risk factor of POPF.The conclusion of this study is similar to that of previous studies[23,31–34].Considering that pancreas texture is one of the major risk factor of POPF and the traditional end-to-side invagination anastomosis cannot avoid chemical leakage due to sutured pancreatic tissue,we tried to find a method which could effectively reduce the risk of pancreatic leakage because of the soft pancreatic texture.

耳鼻咽喉科ESS手术后术腔黏膜的恢复一直是临床医生关注的重点，其中瘢痕和粘连的形成是影响预后的重要因素。少数瘢痕体质的患者术区瘢痕化严重影响鼻腔黏膜的正常功能，使手术不能达到预期的治疗效果；又有部分患者因窦口黏膜瘢痕收缩导致窦腔狭小，甚至再度封闭，分泌物无法排出，反复扩张窦口又会损伤黏膜纤毛功能并加重瘢痕的增生，最后导致鼻窦炎复发。粘连容易引起鼻腔狭窄、结构异常、气流动力学改变、通气异常等，这既不利于鼻腔鼻窦分泌物的排出，又会改变鼻腔的正常生理结构，引起患者术后不适。耳鼻咽喉科常采用反复术后换药、切除瘢痕、分解粘连及糖皮质激素全身或术腔局部给药等方式来解决这类问题。

There are several risk factors for a pancreatic fistula after an end-to-side duct-to-mucosa PJ.Firstly,the physiological role of pancreatic juice is mainly to digest proteins and fat.Therefore,it is easy to destroy anastomotic healing.Secondly,if the pancreatic duct is small,using the method of duct-to-mucosa anastomosis to complete the PJ is difficult and the accessory pancreatic duct or other small pancreatic ducts would be left outside of the jejunum,resulting in a POPF.Considering the risk factors of POPF after the duct-to-mucosa PJ,many scholars conducted a large number of clinical studies to evaluate the pancreatic jejunum invagination anastomosis[1,23–26],and considered the invagination PJ to be a safe and feasible reconstruction method after a PD[27–30].In recent years,based on clinical practice,many experts have made useful improvements on invagination PJs[1,24–26].

渗漏是房屋建筑施工中比较常见的问题，而发生渗漏的位置有很多，如外墙、屋面、门窗、厨卫等，渗漏不仅会对房屋建筑的外观带来极大影响，同时还会影响到房屋建筑的稳定性，降低了房屋建筑的使用寿命，所以在房屋建筑施工中合理的应用防渗漏技术是十分重要的。

Statistical analysis

Statistical analysis was performed with SPSS 18.0(SPSS Inc.,Chicago,IL,USA).Data were expressed as mean±SD or number(%).Continuous variables were compared using Student’s t test.Chi-square test was used to assess the statistical signi ficance of the differences in the frequency distribution of categorical variables.Mann–Whitney U test was employed to analyze the ordinal data.To evaluate the factors associated with POPF rate,we used the unconditional logistic regression model to calculate the odds ratios(ORs)and their 95%con fidence intervals(CIs).Factors signi ficantly associated with POPF in the univariate analysis were subjected to stepwise multivariate regression analysis to obtain independent factors.All statistical analyses were two-sided and P＜0.05 was considered statistically signi ficant.

Results

In the 335 patients,34.0%were diagnosed with distal bile duct carcinoma,26.3%with duodenal papillary carcinoma,16.1%with carcinoma of the pancreatic head,and 14.3%with ampullary carcinoma.The remaining patients were diagnosed with either rare malignancies or benign diseases,such as pancreatic head invasion by carcinoma of the gallbladder with lymph node metastasis,duodenal papillary adenoma with high-level neoplasia.

As previously noted by Kennedy and Yeo[7],the bene fits of the invagination approach can only be generalized in the setting of a meticulous technique.We also agree that any technique,if improperly executed,could result in a poor outcome.Although a multicenter randomized control trial is required to further assess the bene fits of this method,our present study has shown that the suspender PJ is an effective and convenient method.It leads to a lower POPF incidence rate.

If the jaundice of patient lasted over 3 weeks and total bilirubin was greater than 150μmol/L,we used percutaneous transhepatic cholangiodrainage or endoscopic nasobiliary drainage to decrease the total bilirubin to less than 85.5μmol/L before operation.There were no statistical signi ficance in clinical characteristics of patients between the two groups,including the age,gender,BMI,diabetes mellitus,pathological diagnosis,obstructive jaundice,preoperative total bilirubin,albumin,prothrombin time,platelet,hemoglobin and hospitalization duration between the two groups(Table 1).

As it is well-known that the POPF incidence was closely related to the pancreatic texture,we introduced suspender PJ in September 2010 aimed to decrease the POPF.The key steps of the suspender PJ and its essential difference from the traditional end-to-side invagination PJ are shown in Figs.1 and 2.

The overall complications rate was 51.9%(174/335)and the mortality rate was 2.4%(8/335).The top three of the most common complications were abdominal cavity effusion and infection(79/335,23.6%),delayed gastric emptying(51/335,15.2%),and alimentary tract hemorrhage(44/335,13.1%).Overall,POPF was the fourth most common complication(37/335,11.0%),with an incidence rate higher than that of the abdominal cavity hemorrhage(24/335,7.2%).We also evaluated the association of these complications.We found that POPF was a risk factor for both postoperative abdominal cavity infection(OR=8.34,95%CI:3.99–17.42,P＜0.001)and abdominal cavity hemorrhage(OR=4.86,95%CI:1.92–12.33,P=0.001).

Fig.2.Sketch map of suspender pancreaticojejunostomy.

Table 1 Clinical characteristics of patients in traditional end-to-side invagination PJ and suspender PJ groups.

PJ:pancreaticojejunostomy.

Characteristics Total patients(n=335) Traditional PJ(n=147) Suspender PJ(n=188) P value Age(yr) 56.2±10.1 56.6±10.2 55.9±10.0 0.517 Gender 0.314 Male 211(63.0%) 97(66.0%) 114(60.6%)Female 124(37.0%) 50(34.0%) 74(39.4%)BMI(kg/m2) 22.9±2.9 22.9±3.2 22.9±2.8 0.948 Diabetes mellitus 52(15.5%) 20(13.6%) 32(17.0%) 0.394 Pathological types 0.764 Distal bile duct carcinoma 114(34.0%) 51(34.7%) 63(33.5%)Duodenal papillary carcinoma 88(26.3%) 38(25.9%) 50(26.6%)Carcinoma of pancreatic head 54(16.1%) 26(17.7%) 28(14.9%)Ampullary carcinoma 48(14.3%) 22(15.0%) 26(13.8%)Ampullary benign diseases 21(6.3%) 6(4.1%) 15(8.0%)Other rare malignancies 10(3.0%) 4(2.7%) 6(3.2%)Pancreas texture 0.573 Soft 66(19.7%) 31(21.1%) 35(18.6%)Normal 269(80.3%) 116(78.9%) 153(81.4%)Obstructive jaundice 260(77.6%) 118(80.3%) 142(75.5%) 0.302 Preoperative total bilirubin(μmol/L) 170.9±134.9 186.5±143.2 158.9±127.2 0.071 Albumin(g/L) 39.7±4.0 39.4±4.1 40.0±3.8 0.154 Prothrombin time(s) 11.4±1.0 11.4±1.0 11.4±1.1 0.686 Platelet(×109) 257.3±90.5 255.8±89.8 258.5±91.3 0.784 Hemoglobin(g/L) 121.7±17.0 123.4±16.6 120.5±17.2 0.126 Hospitalization time(d) 21.5±12.7 21.7±14.5 21.4±11.2 0.815

Because the POPF could increase the risk of abdominal cavity infection and hemorrhage,we analyzed the associations between clinical characteristics and the occurrence of POPF by the univariate logistic regression model in the two groups.As shown in Table 2,the univariate analysis indicated that in the traditional PJ group,pancreatic texture(soft vs normal)was signi ficantly associated with POPF(P=0.008).However,in the suspender PJ group,the pancreatic texture was not signi ficantly associated with POPF.We further strati fied the patients according to pancreas texture and re-evaluated the association between pancreas texture and POPF.Compared with the traditional PJ,the suspender PJ was still a signi ficant protective factor for the incidence of POPF in the patients with different pancreatic textures.Furthermore,we also found that the traditional PJ and suspender PJ groups had signi ficantly different POPF grades(P＜0.001).The former had a higher incidence of grades B and C POPFs than the latter(Table 3).

Table 2 Univariate analysis of factors associated with POPF in traditional PJ and suspender PJ groups.

Logistic analysis showed that pancreas texture associated with the pathological diagnosis both in traditional PJ group(OR=1.746,95%CI:1.189–2.563,P=0.004)and suspender PJ group(OR=1.514,95%CI:1.103–2.079,P=0.010).

Factors Traditional PJ Suspender PJ OR(95%CI) P value OR(95%CI) P value Age(＞40 vs≤40 yr)1.000 0.828(0.098–6.987) 0.862 Gender(female vs male) 0.782(0.316–1.937) 0.595 1.029(0.280–3.776) 0.966 BMI(≥24 vs＜24 kg/m2) 1.604(0.678–3.796) 0.282 3.103(0.843–11.426) 0.089 Diabetes mellitus 2.143(0.739–6.216) 0.161 1.225(0.248–6.058) 0.803 Pathological diagnosis(carcinoma of pancreatic vs other periampullary lesions) 1.291(0.405–4.110) 0.666 – 1.000 Preoperative total bilirubin(＞85.5 vs≤85.5 μmol/L) 1.934(0.805–4.648) 0.140 1.618(0.452–5.794) 0.460 Preoperative biliary drainage(yes vs no) 1.122(0.461–2.729) 0.800 0.520(0.142–1.907) 0.324 Preoperative albumin(＜35 vs≥35 g/L) 0.520(0.112–2.410) 0.403 2.368(0.465–12.061) 0.299 History of previous abdominal surgery(yes vs no) 0.452(0.126–1.620) 0.223 1.883(0.462–7.670) 0.377 Surgical methods(classic Whipple vs pylorus-preserving) - 1.000 0.395(0.081–1.915) 0.249 Pancreatic texture(soft vs normal) 0.291(0.118–0.719) 0.008 0.511(0.125–2.085) 0.350–

Table 3 The grade of POPF in traditional PJ and suspender PJ groups.

POPF grade Total patients(n=335) Traditional PJ(n=147) Suspender PJ(n=188)Grade A 3(0.9%) 1(0.7%) 2(1.1%)Grade B 23(6.9%) 15(10.2%) 8(4.3%)Grade C 11(3.3%) 11(7.5%) 0

Discussion

白糖不仅有增甜的作用，还有一部分祛腥的作用，同时它又是非常温和的，不像醋的性味那样过烈，会影响海鲜自身的鲜美。难怪有人评价说，白糖可以当味精来用，为菜品增鲜。

以专题项目为载体，模块化重组教学内容，将教学线与实践线各阶段对应的知识点以子项目的方式向学生呈现，将学生要完成的任务根据实际数据库的设计和开发过程划分为8个子项目，如表1所示。

In this study,we observed that the abdominal cavity effusion and infection were the most frequent postoperative complications,followed by delayed gastric emptying,alimentary tract hemorrhage,POPF and abdominal cavity hemorrhage.Moreover,the statistical analysis indicated that a postoperative abdominal abscess and postoperative intra-abdominal hemorrhage were signi ficantly correlated with POPF.As reported in previous studies[17–19],pancreatic juice erodes the surrounding tissues and causes the rupture of blood vessels(intra-abdominal bleeding)8–35 days after a PD.Fourteen patients developed erosive bleeding after POPF in our study.Peng et al.[20]considered that due to injuries on the pancreatic parenchyma and minor ductus pancreaticus caused by a needle and thread during a pancreaticenteric anastomosis,the POPF was inevitable and even a very minor POPF could cause a severe POPF.A number of recent studies re-evaluated the effect of a routinely used octreotide in accordance with grading of pancreatic leakage.However,there is no additional advanced clinical evidence that has shown that octreotide can reduce the risk of pancreatic leakage and other complications after a PD[21,22].Therefore,a reasonable reconstruction of the digestive tract remains the most important factor affecting POPF incidence.

With the improvements in the PJ procedure,the overall incidence rate of POPF has decreased signi ficantly.However,based on the data from several single-institution studies,the POPF incidence rate remains very high,ranging from 3%to 45%,which makes it the most harmful complications after PD[3,12–16].

Pancreatic stump reconstruction methods include a pancreasstomach anastomosis and pancreatic-jejunostomy anastomosis.The PJ was the earliest method and is currently the most widely used one.Because of the rich blood supply of the jejunum and the high mobility of the jejunum mesentery,the jejunum can easily be anastomosed to the pancreas stump.Thus,the PJ is used in a variety of PDs.

Currently,the basic methods of the PJ include the pancreatic duct to jejunum mucosa anastomosis(duct-to-mucosa anastomosis)and the invagination PJ.The latter can be divided into an end-to-end invagination PJ and an end-to-side invagination PJ.Whether the invagination anastomosis is better than the duct-to-mucosa anastomosis remains inconclusive.Bassi et al.randomized 144 patients undergoing the PD to either the twolayer duct-to-mucosa PJ group or the single-layer end-to-side invagination PJ[11].There were no signi ficant differences between two groups with regards to abdominal complications,abdominal fluid collections,or length of hospital stay.However,a dual institution trial by Berger et al.[23]randomized 197 patients to either a two-layer duct-to-mucosa PJ or a two-layer end-to-side invagination PJ.The POPF rate in the duct-to-mucosa group was 24%,while the rate in the invagination group was only 12%(P＜0.05).

The choledochojejunostomy and the gastroenterostomy in operation procedure were routinely performed as described previously[9,10].The only difference between the two groups was the method of the PJ.No other aspect of the intraoperative and postoperative management of the patients was different.Prophylactic octreotide was used in all patients.The traditional end-to-side invagination PJ was performed as previously reported[11],and the pancreatic duct stents were routinely placed.

Our team has implemented the practice of traditional invagination PJ.The POPF incidence in traditional invagination PJ group was 18.4%.It is similar to the rates reported in the literature[23].We analyzed the technical characteristics of the traditional invagination PJ.The pancreas stump was completely invaginated and embedded in the intestine.This could avoid the shortcomings of duct-to-mucosa PJ which could induce the leakage of an accessory pancreatic duct or other small pancreatic ducts not embedded in the intestine.However,we found that the traditional invagination PJ has some drawbacks too.

通过在教材中渗透“数学建模思想”，培养学生的数学应用意识与能力。在教学内容的安排上考虑：第一，让学生认识到每一个数学概念、公式、定理。从广义上说都是数学模型，如从实例中抽象出导数概念即给这类问题建立了数学模型；第二，让学生了解数学建模的方法和过程。教材从经济函数关系的确定到经济问题的建模求解，应给出分析和说明；第三，课程末另设专篇介绍综合运用数学知识建模的几个范例，培养学生初步应用数学建模的创造能力，同时为参加数学建模大赛做好准备。

All patients were subjected to either a classic Whipple procedure or pylorus-preserving PD.The resection range of each PD contained 50%of the distal stomach(need not for pyloruspreserving PD),the duodenum,the head and the uncinate process of the pancreas,gallbladder,and common bile duct.If it was a malignancy,the lymph nodes of station No.3,No.4,No.5,No.6,No.8,No.9,No.12,and No.13a were resected according to the Japanese Society of Biliary Surgery classi fication[8].

Our clinical practice showed that a suspender PJ does not need a “substantial suture”of the pancreatic stump and jejunum.By virtue of bonding and adhesion,the pancreatic stump and jejunum were able to form a stable anastomosis.Compared with the traditional end-to-side invagination PJ,the suspender PJ method has several advantages.Firstly,the procedure is fast and easy.It usually takes approximately 5 min to complete the PJ.Secondly,regardless of the pancreas texture,pancreatic duct diameter and pathologic origin (bile duct/ampulla/duodenum),this method can be well finished,particularly when the pancreatic remnant stump is soft and the pancreatic duct is small.And the incision in the jejunum could be readily designed according to the size of pancreatic stump,which ensure a smooth invagination of the pancreatic stump into the jejunum.Additionally,because the pancreatic stump is completely invaginated into the jejunum,small pancreatic leakage to the outside of the jejunal lumen,including POPF caused by stitching the pancreatic gland,can be avoided.Finally,it is easy to find the POPF during the opertation by injecting physiological saline into the jejunal lumen through the hole where the extra-pancreatic drainage tube out from during the operation.

A total of 263 patients(78.5%)received the classic Whipple procedure,and 72 patients(21.5%)received the pylorus-preserving procedure.The median operative time was 260 mi(150–360).The median volume of blood loss during the operations was 300 mL(100–2000).The mean postoperative hospital stay was 21.5±12.7 days(7–147).The demographic and clinical characteristics of the patients in the traditional end-to-side invagination PJ and suspender PJ groups are detailed in Table 1.

Contributors

JXQ proposed the study.LB and XC performed the research and wrote the first draft.QZQ collected and analyzed the data.LB,XC and QZQ contributed equally to the article.LC,YB and LXJ guided the writing.All authors contributed to the design and interpretation of the study and to further drafts.JXQ is the guarantor.

Funding

None.

Ethical approval

Not needed.

Competing interest

No bene fits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

Acknowledgment

We thank Qi Zhang and Pei Zhan for assistance with the statistical analyses and Xiao-Bin Wu for assistance on drawing the figures.

孟子认为，对待他人的爱和敬是每个人天然本有的。因此，在人与人交往中“其待我以横逆”之时，孟子强调再三反躬自省自身的不足。可以看到，这便与孔子所持的“以直报怨，以德报德”的态度有所区别。

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