Introduction

Portal annular pancreas (PAP), also called circumportal pancreas, is a rare (0.8–2.5%) maldevelopment of pancreas characterized by portal vein completely surrounded by pancreas tissue [1, 2]. Depending on the relationship of the pancreatic duct with the splenic vein, it is distinguished between suprasplenic, infrasplenic, and mixed variants [3]. The classification by Josef P is based on the location of the pancreatic duct with respect to the portal vein [4]. PAP is often (up to 29%) combined with different variants of the anatomy of the arteries, mostly structural variants of the celiac trunk and its branches [1, 5]. Non-standard anatomy, the presence of two possible sources of postoperative pancreatic fistula (POPF), variations in the location of the pancreatic duct, and frequent combinations of PAP with anatomic arterial variations increase the risk of complications during both pancreatoduodenal resection and distal resection of pancreas [6].

In a research by Japanese authors made in 2021, both PAPs they report on were diagnosed intraoperatively and then their presence was retrospectively confirmed by preoperative CT images. In the first case, an open pancreatoduodenal resection for papilla of Vater tumor was performed and the postoperative period was complicated with POPF. In the second case, an open distal resection of pancreas for pancreas cancer was performed and the patient was discharged without complications [7].

In an overview published in 2021, in case PAP is detected during the distal resection of pancreas, it was recommended to perform the transection of both the ventral and the dorsal portions of pancreas at the level of the portal vein using an endoscopic cutter stapler, which can decrease the risk of significant POPF. The authors conclude that each surgeon specialized in pancreas pathology may have to deal with PAP and should be able to recognize it, highly desirable, at the preoperative stage [8].

Case report

A 33-year-old woman presented to the hospital with a neoplasm in the pancreas body. When asked about her complaints, she noted periodic nausea. Her past medical history included laparoscopic cholecystectomy for gallbladder polyps in 2020. The neoplasm in the pancreas was detected in 2019 during the abdominal ultrasound. According to the intravenous contrast MRI data, a round-shaped cystic-solid mass with clear contours, 27x26 mm in size, with septa accumulating contrast agent was detected in the pancreas body (Fig. 1A). The solid component of the neoplasm limits the diffusion of water molecules (Fig. 1B). The pancreatic duct is not extended. A vascular anomaly is noted: common hepatic artery is departed from the superior mesenteric artery.

Fig. 1. MRI of the abdomen, axial scans.

a — contrast-enhanced cystic-solid pancreatic tumor 27×26 mm, venous phase; b — DWI, more intense signal of solid component (arrow); c — retrospective analysis of MRI images revealed that portal vein (arrow) is completely surrounded by pancreatic parenchyma (portal annular pancreas).

The routine laboratory tests showed no deviations. The level of tumor markers was also normal (CA19-9, CEA).

The cytological examination of the fine-needle aspiration biopsy material demonstrated the tubulopapillary hyperplasia of ductal epithelium with dysplasia.

On January 28, 2022, the patient was operated on under general anesthesia with muscle relaxation in dorsal position. Five-port laparoscopic approach was used.

The gastrocolic and the splenocolic ligaments were divided and the stomach was suspended. The serosa was cut above and under the pancreatic isthmus, body, and tail. Then, the distal part of the pancreas was partly mobilized from the retroperitoneum. After that, both the superior mesenteric/portal vein and the splenic vessels were found. The common hepatic artery was not visualized due to an arterial abnormality (departed from the superior mesenteric artery).

The pancreatic isthmus was divided using a stapler (60 mm). We were surprised to find the additional tissue of the pancreas behind the portal vein (Fig. 2A). The dorsal part of the pancreas was divided using a stapler, too. The pancreatic body and tail were mobilized from the retroperitoneum and the splenic hilum with preservation of the splenic vessels. The distal pancreatectomy with preservation of the spleen and splenic vessels was done (Fig. 2B). The resected specimen was removed using an extraction bag.

The operative time was 420 min, and the blood loss was 30 mL.

Immediately after the operation, the MRI images (Fig. 1C) and the literature data were studied. The portal vein was retrospectively found to be completely surrounded by pancreatic parenchyma (PAP), which was detected by neither us nor radiology specialists prior to the surgery. The pancreatic duct was visualized in the front portion of the pancreas (type III according to Joseph). With respect to the splenic vein (the classification by Karasaki), the suprasplenic type was determined.

The postoperative period was complicated by the pancreatic fistula B. The pancreatic amylase level in drainage was 44,284 U/mL (in blood serum, it was 18 U/mL). The patient was discharged on the 6^th day with a drainage volume of up to 30 mL. On the 15^th day, hyperthermia was noted during instrumental examination with no accumulation of fluid in the abdominal cavity, and the antibiotic therapy was initiated. The drain system was removed in an outpatient setting on the 25^th day after surgery as drainage stopped and the absence of fluid in the abdominal cavity was determined by ultrasound.

Pathomorphological conclusion: In the tissue of the pancreas, a 20 mm cystic neoplasm is observed; in its wall, there is an overgrowth of a solid and papillary tumor consisting of medium-sized cells with eosinophilic cytoplasm and hyperchromatic nuclei. In the resection edges, there are no tumor cells. To verify the diagnosis, the immunohistochemical was performed. Results. Tumor cells express CD56, PR, CD99 (dot-like), CK18 (focally), Alpha-1-antichymotrypsin (in a part of cells), Alpha 1-antitrypsin, and vimentin. The nuclear cytoplasmic expression of beta-catenin can be seen focally, predominantly at the edge of a specimen. The proliferative activity index of tumor cells Ki-67 is 6%. In tumor cells, there is no expression of chromogranin A, synaptophysin, and CK7. The morphological and immunohistochemical characteristics of the neoplasms in the pancreas are consistent with the diagnosis of solid pseudopapillary tumor.

It is noteworthy that, with the experience of not less than 2,000 operations on the pancreas with the pancreatic parenchyma transection at the level of isthmus, we have never found such an anomaly. In addition, the retrospective analysis of 649 abdominal X-ray CT images showed PAP in only two patients, which was 0.3%. The analysis included the studies performed from May 1, 2021 to October 1, 2021 using a Toshiba Aquilion Prime 160 computed tomography device in helical scan mode with the slice thickness of 0.5 mm natively and with subsequent four-phase contrasting with a non-ionic X-ray contrast iodine-containing preparation. For the assessment of the presence of the anomaly and length of the circular coverage of the main trunk of the portal vein with the pancreatic tissue, multiplanar reformations of the images to the portal phase using the MIP technology (maximum intensity projections) were used. In total, 703 tomograms were studied but 54 studied were excluded from the analysis due to the impossibility to correctly interpret the presence of this anatomic variant caused by pancreatic necrosis or inflammatory changes in surrounding tissues (n = 27); previous surgeries (2); portal vein thrombosis (n = 7); tumor lesion of the portal vein, pancreas, or surrounding lymph nodes (15); and research defects (n = 3).

Discussion

Annular pancreas (pancreatic parenchyma circularly surrounding the duodenum) is a widely known pancreatic maldevelopment, which is often accompanied by duodenal obstruction causing the necessity of careful examination to find the reason impeding the passage of gastric contents. On the contrary, portal annular pancreas, when the pancreatic tissue completely surrounds the portal vein, as a rule, has no clinical manifestation; it is lesser-known and rather often (52.9%) detected only intraoperatively inspite of the routine preoperative abdominal CT/MRI examination [9]. PAP is a congenital anomaly; the possibility of its occurrence is explained by the fact that the pancreas is formed in the embryonic period by the fusion of two endodermal primordia: the dorsal (a part of the pancreatic head, body, and tail) and ventral (a part of the pancreatic head and uncinate process). During the embryogenesis, they are joined together at the level of isthmus in front of the portal vein. Due to the insufficient turn of the ventral primordium and/or its hypertrophy, the ventral and the dorsal primordia additionally join together behind the portal vein, which leads to the complete surrounding of the portal vein with the pancreatic parenchyma [10]. Joseph P et al. described three variants of PAP based on the location of the main pancreatic duct. In the first type, the main pancreatic duct is located retroportally, in the abnormally formed part of the pancreas. In the second type, each portion of the pancreas has it own rather pronounced duct. In the third type, which is the most frequent, the main pancreatic duct is located anterior to the portal vein [4]. There are data on the annular main pancreatic duct; in the variant, the front and the back parts of the duct have a inextricable connection of the duct system to the right and left from the portal vein [11.]. In terms of the relationship of the parenchyma to the splenic vein, it is distinguished between the suprasplenic (type A), infrasplenic (type B), and mixed (type C) variants [3].

The retrospective analysis of the X-ray data of 1,000 patients performed by John R et al. showed PAP in 25 (2.5%) of them. The criterion of the PAP identification was the complete surrounding of the portal vein with pancreas in two or more slices during the examination by sectional imaging [2]. To our opinion, such high frequency of PAP raises questions. It cannot be excluded that radiation diagnosticians not always can say is there is true fusion of the uncinate process with the pancreatic body or they are closely adjacent to each other. In our experience of more than 2,000 operations on pancreas during twenty years, not a single case of this kind was observed. In addition, we have reproduced the experience of John R and analyzed medical images of 649 patients, and PAP was detected in tomograms of only two patients (0.3%).

The results by Yilmaz E seem more realistic: the reported frequency of PAP is 0.8% (n = 55 of 6813). Abnormal arterial anatomy occurred in 16 patients (29%); the most frequent (n = 6) was the variant where the common hepatic artery was departed from the superior mesenteric artery [1]. Note that, in our case, PAP was also combined with vascular anomaly: common hepatic artery is departed from the superior mesenteric artery.

According to the review published in 2015, where 91 case of PAP was described, including fourteen patients undergoing pancreatic surgery, the presence of such anomaly increases the risk of pancreatic fistula after both pancreatoduodenal resection and distal resection of pancreas. Frequent combination of the anomaly of the pancreas with arterial anatomy variations of the celiac trunk and its branches additionally complicates the surgery and is associated with risks [6.] Yuan H described a case of a successful open operation for cancer of distal part of pancreas in a patient with PAP and the absence of celiac trunk. In that work, unfortunately, there is no description of the method of treatment of pancreas resection edges; based on the presented intraoperative pictures, the ligation of the back part of PAP can be supposed. The author noted the absence of postoperative complications; the patient was discharged on the 11^th day after the surgery [5]. To try to decrease the risk of POPF, Kuriyama N, based on the literature data and his own experience, assumes that discission of parenchyma of PAP is possible more distal than isthmus if the parenchyma thickness is less than 12 mm. If the parenchyma thickness at the level of the pancreas body in the zone of possible discission is more than 12 mm, the risk of fistula increases and, in this case, the transection of the isthmus and the retroportal part of PAP is preferable. Despite the fact that two sources of possible formation of PAP appear, lower injury rate of each discission seems more preferable. The author included into the overview 7 patients including his observation of distal resection of pancreas in the presence of PAP; IIIA PAP were predominant (71.4%, n = 5). Two resections, one of which was the author’s case, were performed laparoscopically. Five patients developed POPF grade A or B (71.4%) including that in the clinical case described by Kuriyama N [12]. According to the overview by Pandrowala S et al. published in 2021, in case PAP is detected during the distal resection of pancreas, it is recommended to perform the transection of both front and back portions of pancreas at the level of the portal vein using an endoscopic cutter stapler. Six distal resections of different extent and one median resection of pancreas are presented. The authors do not recommend to transect the pancreas in more distal direction due to thicker parenchyma there, which leads to crushing pancreatic parenchyma and higher risk of POPF. The authors consider that it is more preferable to treat two thinner slices of pancreas than one thick one. Also, in the authors’ opinion, the transection of parenchyma using ligation is undesirable, because causes the risk of more frequent development of pancreatic fistulas. It is not recommended to excise the abnormal part of the pancreas in the distal resection due to the unneeded increase of the extent of surgery and the risk of damage of hepatic artery or celiac trunk. The authors admit the limitations of their study caused by the retrospective nature of the review with a small number of patients. However, they conclude that each hepatopancreatobiliary surgeon should know the signs of PAP and features of the technique of the surgical intervention in case of this anomaly [8].

In the case we present here, PAP was not recognized at the preoperative stage because we were unfamiliar with such anatomic variant. During the surgery, the location for the transection of the pancreas parenchyma at the isthmus was chosen because of the close location of the tumor in the pancreatic body and, in addition, this was indeed the narrowest part of the pancreas. For the transection of pancreatic parenchyma in front of the portal vein, a stapler was used, which is done routinely during both open and laparoscopic distal resections for the past several years.

After the transection of the pancreatic isthmus, we were surprised to see a hypertrophied uncinate process spliced with the pancreatic body, i.e., PAP (Fig. 2A). Fortunately, it was the suprasplenic type, without the surrounding of the superior mesenteric vein and/or splenic vein with pancreatic parenchyma. We had no choice but to incise the retroportal part of PAP using a 60-mm stapler (Fig. 2B).

Fig. 2. Intraoperative images.

a — dorsal part of the annular pancreas (thick arrows) is visualized above the splenic vein (thin arrows) after transection of the pancreas at the level of portal vein. suprasplenic type of anomaly; b — dorsal part of the portal annular pancreas is transected. Resection edges are anterior (thick arrows) and posterior (thin arrow) of the portal vein.

The patient was discharged on the 6^th day with drainage left because of POPF. Due to hyperthermia, on the 15 day after the surgery, oral antibiotic therapy was prescribed in the outpatient setting (POPF grade B). The drain system was removed on the 25^the day after the surgery as drainage stopped.

Conclusion

PAP is a rare and lesser-known maldevelopment of pancreas. In addition, it is asymptomatic. Thus, it is unfamiliar to practicing surgeons, and it is not attempted to identify this anatomic variant during the study of sectional images. In a half of cases (53%), PAP is an unpleasant surprise during an operation on the pancreas, as it occurred in our observation. The anatomy variation of the arteries of the celiac trunk often accompanies PAP. While planning an operation on the pancreas, in particular, the distal resection of pancreas, the probability of PAP should be considered. If this anomaly is detected before or during the operation, the preference should be given to the transection of the pancreas at the level of the portal vein using a stapler. At the first stage, the front part of the pancreas (i.e., isthmus) is transected; at the second stage, the retroportal part of PAP is transected. This approach is aimed at reducing the risk of POPF. The ligation or extirpation of the retroportal part of PAP is undesirable during the distal resection of pancreas due to higher injury rate and higher risk of clinically significant POPF.

The authors declare no conflicts of interest.