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0 1990 The Japanese Society of Pathology

I m m u no his to c hem ica I a nd G ro s s D i ssec t io n Studies of Annular Pancreas

Koichi Suda

Three cases of annular pancreas were studied immunohis- tochemically on an embryological basis in relation to the duct system. Annular pancreatic tissue was characterized by abundant, irregularly shaped islets with a very high proportion of pancreatic polypeptide (PP) cells, similar to those in the postero-inferior part of the pancreatic head of controls. This PP-rich area fused with PP-poor areas in both the anterior and posterior portions, resulting in encir- clement of the duodenum except for a few PP-poor areas. The pancreatic duct of the annular tissue passed from the anterior portion to the lateral and posterior portions, finally joining with the main pancreatic duct. No connection was present between the duct of the anterior portion and the main pancreatic duct. Therefore, the annular pancreatic tissue was revealed to arise from the ventral primordium, supporting Lecco’s theory that the free end of the ventral anlage is fixed. Acta Pathol Jpn 40: 505-508, 1990.

Key words : Annular pancreas, Pancreatic polypeptide-rich area, Ventral anlage

INTRODUCTION

Annular pancreas consists of a collar or ring of pancre- atic tissue surrounding the second part of the duodenum and continuing into the head of the pancreas on either side. The gut lumen is usually narrowed.

A number of theories (1-3) have evolved to explain the formation of annular pancreas on an embryological basis. Lecco(2), whose theory is perhaps the most widely accepted, postulated that if the free end of the ventral anlage is fixed, it will be drawn around the right side of the duodenum to fuse with the head of the pancreas, thus encircling the duodenum. According to Tieken(3), the condition is caused by two ventral an-

Received December 13, 1989. Accepted for publication February 21, 1990. Department of Pathology, Yamanashi Medical University, Y a manas hi, Japan. Mailing address : Koichi Suda (?RE@#-), Department of Pathology, Yamanashi Medical University, Tamaho, Naka- koma, Yamanashi 409-38, Japan.

lagen fusing with the dorsal anlage to form a ring around the duodenum. Baldwin (l), on the other hand, suggest- ed that persistence of the left ventral anlage, which normally atrophies, is responsible. However, none of these theories is thought to explain the phenomenon in all cases.

In this study, I tried to explain the development of annular pancreas based on pancreatic anlagen and the pancreatic ductal pattern.

MATERIALS AND METHODS

Specimens from three patients (64yr, F; 7y r , F; 5 days, F) with annular pancreas who were operated on or autopsied at Y a ma nas hi Medica I U niversit y, Y ama nas hi, and Juntendo University, Tokyo, were studied using macroscopic and immunohistochemical techniques. In addition, non-cancerous pancreatic tissues from ten pancreato-duodenectomy specimens, selected randomly from our case records for 1988, were also investigated as a control group. The pancreatic tissue, including the annular tissue, was fixed in formaldehyde solution, dehy- drated and embedded in paraffin. Histologic sections were stained with hematoxylin-eosin and Grimelius, and immunostained with anti-pancreatic polypeptide (PP; UCB Co.), which reacts selectively with cells in the ventral pancreas (4). Furthermore, anti-insulin, anti- glucagon and anti-somatostatin (all from DAKO Co.) were used. For immunostaining, the following proce- dure was used. The sections were treated with 0.3% hydrogen peroxide to block endogenous peroxidase and immersed in 0.01 M phosphate-buffered saline (PBS), pH 7.2, for 10-15 min. After exposure to non-immunogoat serum, the sections were first treated with the above- mentioned antibody at optimal dilution (1 : 200) at room temperature for 30 min, then washed and exposed to goat anti-rabbit IgG at room temperature for 30 min. After rinsing thoroughly with PBS, the sections were incubated with a 1 : 200 dilution of peroxidase-labeled antibody at room temperature for 30 min, and finally

5 06 Annular Pancreas (Suda)

RESULTS incubated with 3, 3’-dia mino benzidine (DAB) containing 0.005% hydrogen peroxide. Appropriate controls were included.

The pancreatic head tissue including the annular tissue was mapped for PP-positive cells.

In all three cases of annular pancreas, the pancreatic tissue completely encircled the duodenum without appar- ent obstruction. In the one surgically resected specimen (Case 1 ; 64 yr, F) (Fig. la) , in which the duct system was studied macroscopically, a pancreatic duct passed

Figure 1. Annular pancreas from a pancreato-duodenectomy specimen (Case 1 ; 64 yr, F). a. Macroscopic appearance of cut surface and distribution of PP islets. PP indicates PP-rich area ; CBD: common bile duct. b. Illustration of the pancreatic duct (arrows) in the annular pancreatic tissue, based on the ventral (VEN) and dorsal (DOR) pancreas. CBD indicates common bile duct ; MPD : main pancreatic duct; PV: Vater’s papilla. AP : accessory papilla.

b

Acta Pathologica Japonica 40 (7) : 1990 507

from the anterior portion of the annular tissue to the lateral and posterior portions, finally joining with the main pancreatic duct (Fig. 1 b). No connection was present between the duct in the anterior portion and the main pancreatic duct. The duct system in the remaining two cases was not studied macroscopically because the specimens were from children. The islets of Langerhans in the annular tissue of the three cases were usually irregular in shape, and characterized by a striking abun- dance of PP cells immunohistochemically (Fig. 2). From the PP-positive cell mapping, these PP-rich areas in the three cases were found to be fused with PP-poor areas (Fig. 3) in both the anterior and posterior portions,

Figure 2. Strikingly abundant PP cells in the annular pancreatic tissue (Case 2 ; 7 yr, F). lmmunostaining for anti PP

Figure 3. Junction (arrowheads) between PP-rich and PP-poor areas in annular pancreas from same patient as in Fig. 2. Immunostain- ing for anti-PP.

and the PP-rich area encircled the duodenum except for a few PP-poor areas, as shown in Fig. l a . Branches of the pancreatic duct in the annular tissue, in which abun- dant PP cells were found, did not extend to the PP-poor area either macroscopically and microsco pica Ily.

In the control cases, the head of the pancreas was clearly separated into two parts as judged from the distribution of irregularly shaped islets, which were stained positively by the Grimelius silver method and heavily immunostained with anti-PP. These islets were distributed selectively in the postero-inferior part of the pancreatic head. No pancreatic ducts communicated between these two parts except for the main duct.

5 08 Annular Pancreas (Suda)

DISCUSSION

The present study showed that annular pancreatic tissue was characterized by abundant, irregularly shaped islets with a very high proportion of pancreatic poly- peptide (PP) cells. This was similar to the description of annular pancreas by Sessa et a/. (5). From the mapping of PP-positive cells in this study, however, this PP-rich area was found to fuse with PP-poor areas in both the anterior and posterior portions, resulting in encirclement of the duodenum except for a few PP-poor areas. In the control specimens the irregularly shaped islets, which were stained positively by the Grimelius silver method and immunostained with anti-PP, were distributed selec- tively in the postero-inferior part of the pancreatic head (4, 6). As to the origin of this distinct part, it is thought to be derived from the ventral pancreatic primordium during embryogensis (6-7). Hence, annular pancreatic tissue arises from the ventral primordium and encircles the duodenum except for a few areas derived from the dorsal anlage.

In one case (64 yr, F), in which the duct system was studied macroscopically, a pancreatic duct passed from the anterior portion of the annular tissue to the lateral and posterior portions, finally joining with the main pancreatic duct. No connection was present between the duct of the anterior portion and the main pancreatic duct. This pancreatic duct pattern was similar to that observed by Ecker(8), and those in Anderson and Wapshaw's review (9) as follows: in 17 of 20 cases of annular pancreas in which the duct system has been studied adequately, the annulus had a single main duct originating in the portion of the ring overlying the left anterior surface of the duodenum, crossing the gut posteriorly from right to left, and opening into the main pancreatic duct close to the ampulla. However, these observations concerned the duct system only. In the present study, both the duct system and the distribution of PP cells were studied simultaneously. From the schematic illustration in Fig. 1 b, the anomalous pheno- menon of annular pancreas can be explained more clearly

as follows: of two fusions between the PP-rich and PP- poor areas, the posterior fusion is considered to be the normal developmental process because of the arrange- ment of the duct system. Accordingly, that of the anterior portion is thought to be anomalously fixed.

Therefore, annular pancreatic tissue was revealed to arise from the ventral primordium, which supporting Lecco's theory that the free end of the ventral anlage is fixed.

Acknowfedgements : The author thanks the Department of Pathology, Juntendo University, School of Medicine, Tokyo, for providing specimens. I am also grateful to Dr. Yoji Yoshida, MD, Professor of Pathology, Yamanashi Medical University, for his kind advice, and to Mr. Charles Randle Allala for reviewing the English manuscript. This work was supported in part by a research grant from the Ministry of Welfare, Japan.

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REFERENCES

Baldwin WM. A specimen of annular pancreas. Anat Rec 4 : 299-304, 1910. Lecco TM. Zur Morphologie des Pancreas Annulare. Sitzungsb Wien Akad Wiss Math-Nat KI 119: 391- 406, 1910. Tieken T. Annular pancreas. Am Med 2 : 826, 1901. Kloppel G and Lenzen S. Anatomy and physiology of the endocrine pancreas. In Kloppel G and Heitz FU, eds. Pancreatic pathology. Churchill Livingstone, New York, 1984: 133-153. Sessa F, Fiocca R, Tenti P, et a/ . Pancreatic polypep- tide rich tissue in the annular pancreas. A distinctive feature of ventral primordium derivatives. Virchows Arch [Pathol Anat] 399: 227-232, 1983. Suda K, Mizuguchi K, and Hoshino A. Differences of the ventral and dorsal anlagen of pancreas after fusion. Acta Pathol Jpn 31 : 583-589, 1981. Rahier J, Wallon J, and Henquin JC. Cell populations in the endocrine pancreas of human neonates and infants. Diabetologia 20: 540-546, 1979. Ecker A. Bildungsfehler des Pancreas und des Her- zens. Z A r t Med Leips 14: 354-356, 1862. Anderson JP and Wapshaw H. Annular pancreas. Br J Surg 39: 43-49, 1951.