Introduction

Chronic pancreatitis with inflammatory head enlargement is generally associated with abdominal pain and/or compression of the surrounding tissues [1, 2]. The traditional operation for the inflammatory head mass was the pancreatoduodenectomy sec. Kausch–Whipple, however, in such a benign disease like chronic pancreatitis, removal of the distal part of the stomach, the entire duodenum, the whole pancreatic head, the gallbladder, the distal part of the bile duct, and the beginning of the jejunum is rarely necessary [3]. Even the pylorus-preserving modification of the Whipple procedure means an overtreatment in this setting. The preservation of the endocrine and exocrine function has a paramount importance in the quality of life of the patients. This purpose guided Beger, who developed a less invasive technique, namely the duodenum-preserving pancreatic head resection (DPPHR). The cause of the symptoms is eliminated by the subtotal resection of the enlarged pancreatic head; moreover, the physiologic continuity of the gastrointestinal and biliary route is preserved, without unnecessarily sacrificing pancreatic tissue. The procedure was associated with lower morbidity, better preservation of the endocrine function, and the quality of life [4, 5]. Since that time, several modifications of the original Beger operation have been introduced, like the Frey and Berne procedures [6, 7]. These aimed to make the procedure easier and shorter, but at the same time to maintain the advantages of the Beger operation. Since then, many trials analyzed and compared these methods to each other, like Beger vs. Whipple [8, 9], Frey vs. Whipple [10, 11], Beger vs. Berne modification [12, 13], Berne vs. Whipple [14], and Beger vs. Frey [15]. According to the studies, all methods are equally effective for the management of the symptoms of chronic pancreatitis with inflammatory head enlargement [8, 10, 11, 14, 16, 17]. The DPPHRs are more advantageous, than the Whipple procedure, regarding the early postoperative outcomes [8, 10, 11, 16], however, concerning the late follow-up results data are conflicting [9, 18,19,20]. Therefore, we aimed to analyze and compare the early and late outcomes of all these procedures in a retrospective study. Moreover, new recommendations about the pancreatojejunal and the biliary anastomosis during DPPHRs were also suggested.

Patients and Methods

Between 1991 and 2021, for symptomatic chronic pancreatitis with inflammatory head mass, 230 pancreatic head resections were carried out, namely 55 Beger, 113 Frey, 16 Berne operations (performed by one surgeon), and 46 Whipple procedures (classic or pylorus-preserving types, performed by another surgeon and rarely by the previous surgeon only in case of a severe duodenal stenosis and strong suspicion of malignancy). Due to its simpler technique, the Frey gradually replaced the Beger operation after 1994, then from 2008, the Berne modification also became an option in the surgical treatment of chronic pancreatitis with head enlargement. Since 2003 in all types of the DPPHR, the pancreatic anastomoses — first recommended by us — were fashioned with a one layer, running suture method. The Whipple procedure (classic or pylorus-preserving) was the method of choice in the case of a severe duodenal stenosis and if the preoperative data and the intraoperative findings raised the strong suspicion of a malignancy. During DPPHRs, the cholestasis was resolved — according to Beger — with an “internal” biliodigestive anastomosis (BDA) by making an opening on the dilated part of the bile duct on the resectional surface. However, in some cases, a recurrent cholestasis was observed after the “internal” BDA. Thus, later on, the safer “external” BDA was preferred, namely an anastomosis was created between the jejunal loop and the extrapancreatic (supraduodenal) part of the common bile duct, in case of a cholestasis during the index operation, as well as at recurrent and later onset cholestasis. In two cases of newly onset cholestasis, an endoscopic biliary stenting was chosen as an option. In four cases of Frey procedures, an inflammatory enlargement of the left part of the pancreas was observed, so a V-shaped excision of the ventral part of the body and tail was carried out [21]. Recently, during Berne operations, the duct of the remnant pancreas was opened shortly (about 2 cm) to create a larger orifice on the pancreatic surface. Intraoperative frozen-section histology of the resected tissues was a routine measure. Operative pictures of the Frey, Berne, and the Whipple procedure (Figs. 1, 2, 3, 4) and an illustration of the Beger operation (Fig. 5) are presented.

Fig. 1
figure 1

Frey procedure — longitudinal opening of the dilated Wirsung’s duct, subtotal head resection (C:cavity, W:Wirsung’s duct, R:rim of the head remnant, P:probe introduced through the papilla Vateri)

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Fig. 2
figure 2

Frey procedure — longitudinal pancreatojejunal anastomosis (D:duodenum, J:jejunum, P:pancreas, A:anastomosis with single layer continuous suture)

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Fig. 3
figure 3

Berne modification — subtotal head resection, one pancreatojejunal anastomosis, the medial row is ready. (D:duodenum, J:jejunum, L:large bowel, C:cavity after subtotal head resection)

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Fig. 4
figure 4

Whipple procedure (pylorus-preserving type) with pancreatojejunostomy (PJ:pancreatojejunostomy, HJ:hepaticojejunostomy, DJ:duodenojejunostomy)

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Fig. 5
figure 5

Beger procedure — after transection of the pancreatic neck, then the subtotal pancreatic head resection, two pancreatojejunal anastomoses (PJ) were carried out (with the permission of Medicina Publisher, Budapest, Hungary, graphic: Mrs. Éva Olgyay)

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The preoperative data, moreover, the early and late outcomes, were analyzed, as well as the late quality of life by the help of a questionnaire, sent to patients operated on after 2007. The pancreas specific items of the Gastrointestinal Quality of Life Index (GIQLI) [22], like the pain, diarrhea, bloating, appetite, body weight, and general satisfaction, moreover, the endocrine function and the presence of the etiological factors (smoking and alcohol consumption) were investigated.

Statistical Analysis

Descriptive statistical tools, such as means, standard deviations, ranges, and frequencies, were used to describe the basic characteristics of the data. To observe differences in the characteristics between the techniques, we applied the Kruskal–Wallis test or the one way ANOVA (in case of age) with the Bonferonni post hoc test. For categorical variables, we applied the chi-square test or the Fisher’s exact test depending on the event number. Statistical significance was set at p < 0.05. All analyses were made with IBM SPSS Statistics v 26.0 software package (IBM’s Corporate, NY, USA).

Results

Table 1 shows the age, gender, and the clinical symptoms indicative for an operation. As an etiological factor, alcohol and/or nicotine abuse was found in about 2/3 of the patients. There were no statistically significant differences between the groups, regarding the age, gender, pain, and cholestasis. However, the duodenal stenosis was most frequent in the Whipple group and the difference was significant between the Whipple and Beger/Frey groups. The rates of the suspicion of malignancy showed the same pattern. Table 2 demonstrates the length of the procedures, the need for transfusion, the length of intensive care unit (ICU), and total postoperative hospital stay. Regarding the length of the procedure and the need for transfusion, the Berne and the Frey operations were statistically more advantageous, than the Whipple and the Beger types. The duration of the ICU and total postoperative hospital stay were significantly shorter after the Berne and the Frey operations, compared to the Whipple one. The intraoperative frozen-section histology revealed chronic inflammation in all but two cases, when a malignancy required a Whipple operation to be performed. Table 2 shows furthermore the rate of early morbidity including the clinically relevant postoperative pancreatic fistulas (CR-POPF), reoperations, and mortality. The early morbidity rate after the Whipple procedures was significantly higher, than after the Frey type. Regarding the CR-POPF, reoperation, and mortality rates, there was no difference between the procedures. Table 3 shows the late results, which were similar in the groups. The Medical Database also supplied some additional information, thus, the late follow-up data were available in a rate of 50–79% (Table 4). The late mortality rates were higher after the analysis of the questionnaires, compared to the Medical Database, while the direct contact with the patients’ family by mail served additional data, which were not included in the local Database, containing only the information from the Clinical Center of the University of Pécs. While from the Beger group only one questionnaire was returned, this was not taken into an account. Table 5 demonstrates the pancreas specific and additional other data, which were similar. The majority of the patients had no pain, the exocrine and endocrine functions were well preserved, and the general satisfaction was excellent. However, most patients did not stop the alcohol consumption and smoking. It could be observed that information was lost due to several reasons, like death, address change, denied answer, etc. Thus, no proper statistical analysis was possible regarding the late results; however, the available data showed that the late mortality rate was obviously the highest after the Whipple procedure (Table 4).

Table 1 Preoperative data
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Table 2 Intra- and postoperative data
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Table 3 Late morbidity, reoperation, and mortality
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Table 4 Follow-up results I
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Table 5 Follow-up results II
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During DPPHRs in cases with cholestasis, the effectiveness of the applied methods was also investigated (Table 6). It could be seen that at Beger procedures, the “internal” BDA was preferred, while in cases of Frey/Berne procedures, the “external” one was mostly performed. The sum of the rate of recurrent and newly onset cholestasis was a bit higher after the Beger, than after the Frey/Berne operations, due to more cases of recurrence following the “internal” BDA (Beger: 7.3% vs. Frey/Berne: 5.4%). After the “external” BDA, the cholestasis never returned.

Table 6 Cholestasis before and after DPPHRs
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Discussion

In chronic pancreatitis, the most common indication for a surgical procedure is the inflammatory enlargement of the pancreatic head, which is associated with severe abdominal pain and/or compression syndrome. For this condition, the Whipple procedure is rarely truly required, except in cases of severe duodenal stenosis or a strong suspicion of malignancy. Beger was the first, who established the principle, that in a benign disease like chronic pancreatitis, it is unnecessary to remove the duodenum, the whole pancreatic head, and to change the physiological route of the food and the bile. By the subtotal head resection, the disadvantages could be resolved; moreover, the endocrine and exocrine functions were better preserved [2, 4, 5]. Modifications of the Beger procedure were introduced later, like the Frey and Berne operation [6, 7]. The fundamental part, namely the subtotal head resection, is common in these procedures. Recent trials found no differences in patient-relevant outcome parameters during the follow-up between the Beger and Berne [13], then between DPPHRs and Whipple procedures [18]. All operations were equally effective in relieving from the symptoms of chronic pancreatitis with inflammatory head enlargement, nevertheless offering advantages regarding the duration of the procedure [18], especially the Berne modification [13].

Similarly to the international trials, our series also showed that all types of procedures (Beger, Frey, Berne, Whipple) were able to improve the patient’s quality of life, but without differences in the long-term outcomes. Regarding the late results, it can be assumed that the mortality rate was probably higher in all groups — especially after the Whipple procedures — due to mainly nonpancreatic diseases, like liver cirrhosis, extrapancreatic malignancies, atherosclerosis, chronic alcoholism, etc. [23]. However, the patients alive had relatively good quality of life.

Moreover, the DPPHRs were more advantageous, than the Whipple procedure, concerning the length of the operation, the ICU, and total postoperative hospital stay. Especially, the Berne operation was superior regarding the duration of the operation and its simplicity [13, 18]. After DPPHRs, redo surgery might be necessary during follow-up, due to the progression of the inflammation in the remnant pancreatic head [18]. In the present series, reoperation was needed in some cases for recurrent (only after “internal” BDA) or newly onset (after any type of DPPHRs) cholestasis. In these instances, the jejunal loop was anastomosed to the extrapancreatic (supraduodenal) part of the biliary duct (“external” BDA), to solve the problem. Therefore, this type of BDA became our method of choice during the index operation and also in the case of a recurrent and newly onset cholestasis, because the cholestasis never returned afterwards. Since 2003, the pancreatojejunal anastomoses were done — recommended by us — in a single layer, running fashion in DPPHRs, without an increase in complications. For the prevention of a possible pancreatic duct stricture on the left resectional surface, it was distally shortly opened during Berne operations.

Summing up, our recommendations are the following: for chronic pancreatitis with inflammatory head enlargement, the Berne modification is the preferred method, made with a pancreatojejunal anastomosis with a single layer running suture technique, after creating a wider opening on the pancreatic duct. The Berne operation is suitable in normal and also in dilated duct disease, while the Frey is rather preferable in cases with a “chain of lakes” phenomenon. In case of cholestasis, an “external” BDA is advisable to prevent recurrent cholestasis and redo surgery. However, in cases when the suspicion of malignancy still exists even after a thorough intraoperative evaluation, or the duodenal stenosis is not resolvable with a Kocher maneuver, the method of choice is the Whipple procedure (classic or pylorus-preserving). One can find a contradiction that our preferred method was performed in the smallest number. The explanation for that is the significantly decreasing number of chronic pancreatitis patients referred for surgery in the last decade, compared to 10 years earlier. The reason might be the social degradation of these people, their drop out from the health care system, early death, or denial of any treatment. This phenomenon serves as a further argument for the preference of a less invasive method, like the Berne modification, which is the simplest and shortest, and at the same time an effective intervention. This essential aspect must be considered, when surgical therapy is needed in these poor-risk, often alcoholic, and smoker patients, who are generally not good candidates for a Whipple procedure. However, improving the quality of life of this patient population — even only for some years — is also our duty.

Conclusion

For the effective treatment of chronic pancreatitis with inflammatory head mass, the duodenum-preserving pancreatic head resections and the Whipple operation are equally suitable. However, there are some special aspects (strong suspicion of malignancy, severe duodenal stenosis, patient’s risk factors and general condition, etc.), which help to choose the adequate type of the head resection most advantageous for the patients.