Surgical Embryology and Anatomy of the Pancreas

SURGICAL ANATOMY AND EMBRYOLOGY

0039-6109/93 $0.00 + .20

SURGICAL EMBRYOLOGY AND ANATOMY OF THE PANCREAS Lee John Skandalakis, MD, FACS, Joseph S. Rowe Jr, MD, Stephen W. Gray, PhD, and John E. Skandalakis, MD, PhD, FACS

HISTORY OF PANCREATIC ANATOMY It is beyond the scope of this article to present a detailed history of the pancreas; however, it is appropriate to touch on some high points. Eristratos (310-250 BC) was the first to mention the pancreas in his writings. In 1532, David Edwardes, who was the first to write an anatomy book in English, suggested that the pancreas provided physical support for the delicate and thin-walled lymphatic vessels. Vesalius, in 1543, mentioned the organ, using its Greek name without further expounding upon it.62 His illustrations purporting to show the pancreas are unintelligible. Wirsung, in 1642, described the main pancreatic duct that bears his name. 65 He thus established the glandular nature of the pancreas. Bidloo, in 1685, was the first to observe the junction of the common bile duct and the pancreatic duct. 6 The enlargement of the lumen (ampulla) and the projection into the duodenum (papilla), first described by Bidloo, were subsequently redescribed by Vater in 1720. Santorini,52 in 1724, described the main and accessory duodenal papillae as major and minor caruncles. In 1889, almost by accident, von Mering and Minkowski discovered that pancreatectomized dogs became diabetic, and that blood glucose was under the control of some substance

From Emory University School of Medicine (LJS, SWG, JES); Veterans Affairs Medical Center (JSR); and Piedmont Hospital (LJS, JES), Atlanta, Georgia; and The Medical College of Georgia, Augusta, Georgia (JES)

SURGICAL CLINICS OF NORTH AMERICA VOLUME 73 • NUMBER 4 • AUGUST 1993

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produced in the pancreas. 44 It was discovered subsequently by Langerhans40 in 1869 that the source of this substance produced in the pancreas was in the islet tissue. De Meyer,2° in 1909, named this hypothetical hormone from the islets "insuline." It was not actually isolated, however, until 1922 by Banting and Best. 3

EMBRYOLOGY OF THE PANCREAS

The decalogue of pancreatic embryogenesis (Figs. 1 and 2) is as follows, keeping in mind of course the two pancreatic primordia, the dorsal and ventral. 1. At the end of the fourth week, 26th day, the dorsal pancreatic primordium arises from the dorsal side of the duodenum. 2. The ventral primordium arises slightly later, 32nd day, from the base of the hepatic diverticulum. 3. Contact between the two pancreatic primordia takes place at about 37 days, and fusion occurs at the end of the sixth week. 4. The ventral primordium is part of the head and uncinate process. 5. With the fusion of the two primordia, both ducts anastomose.

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Do~sal pancreas

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Figure 1. Embryonic development. A, Formation of dorsal and ventral pancreatic primordia. B, Rotation of the ventral pancreas. C, Fusion of the primordia to form adult pancreas. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

SURGICAL EMBRYOLOGY AND ANATOMY OF THE PANCREAS

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Figure 2. Rotation of duodenum and pancreas. A, Primitive relation of dorsal and ventral pancreatic primordia. B, Disappearance of ventral mesentery and rotation of ventral pancreas. C, Final retroperitoneal position of duodenum and pancreas. The plane of fusion of the mesoduodenum is the avascular fascia of Treitz. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:1750, 1979; with permission.)

6. The duct of Wirsung is formed by the duct of the ventral pan-

7. 8. 9. 10.

creas and the distal portion of the duct of the dorsal pancreas and forms the main duct. The duct of Santorini is the proximal duct of the dorsal pancreas. The secretory acini appear during the third month. The islands of Langerhans arise from the acini also at the end of the third month approximately. Critical events of development. Rotation and fusion of the pancreatic primordia are the only critical morphologic events. Malrotation of the ventral primordium in the fifth week results in an annular pancreas. Fusion in the seventh week produces various possible ductal patterns.

Suda et al,56 however, question the classical concept of ansa pancreatica, and hold that an inferior branch of the dorsal pancreatic duct is connected with the ventral pancreatic duct. CONGENITAL ANOMALIES

There are many congenital anomalies of the pancreas (Table 1). This paper cannot present all of them but will discuss some of them briefly. Annular Pancreas

This is a thin, flat band of normal pancreatic tissue surrounding the second part of the duodenum and continuing into the head of the pan-

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Table 1. CONGENITAL ANOMALIES OF THE PANCREAS

Aplasia-hypoplasia Hyperplasia-hypertrophy Dysplasia Variations and anomalies of the ductspancreas divisum Annular pancreas

Pancreatic gallbladder Cystic fibrosis Pancreatic cysts Rotational anomalies Ectopic pancreatic tissue Vascular anomalies

creas on either side (Fig. 3). The band may be partially or wholly free from the duodenum, or the pancreatic tissue may penetrate the duodenal muscularis. The ring of pancreatic tissue contains a large duct that usually enters the main pancreatic duct. This, however, occasionally enters the duodenum independently. How the annular pancreas is developed is not known. Is the ventral anlage totally responsible by its early division in two parts in a way that the left part follows an opposite way, producing the constricting ring? Perhaps, or maybe early fusion of the ventral pancreatic tip with the dorsal is responsible for this anomaly. We do not know. Duodenal stenosis at the level of the pancreatic ring is usual. If obstruction at the site of the annulus exists before birth, hydramnios frequently is present.35 However, half of the patients with annular pancreas do not have symptoms until adulthood. 41 The symptoms are those of duodenal obstruction. Currently, the procedure of choice to treat duodenal obstruction caused by annular pancreas is duodenoduodenostomy, first proposed by Gross and Chisolm.33 Ectopic and Accessory Pancreas It is not unusual to have pancreatic tissue in the stomach, duodenal or ileal wall, Meckel's diverticulum, or at the umbilicus. Less common Portol v.

Figure 3. Annular pancreas. The duodenum under the annulus is usually stenosed. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50,1979; with permission.)

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sites are the colon,12 appendix,I6 gallbladder,37 omentum or mesentery,63 and in an anomalous bronchoesophageal fistulaS (Fig. 4). Most ectopic pancreatic tissue is functional. Islet tissue often is present in gastric and duodenal heterotopia, but it is usually absent in accessory pancreatic tissue elsewhere in the body. Duodenal accessory pancreas may be lobules of normal pancreas in the submucosa sequestered beneath the muscularis externa. In other cases pancreatized Brunner's glands may be considered to be a potential anlage. This is suppressed normally by the earlier maturing normal pancreas that may occasionally escape from such suppression. Feldman and Weinberg28 found duodenal pancreatic tissue in 13.7% of 410 necropsy specimens. Pearson47 estimated that heterotopic pancreatic tissue could be found in as many as 2% of autopsies if it were sought carefully. About 6% of Meckel's diverticula may be expected to contain pancreatic tissue. 19 Atypical metaplasia of pluripotential endodermal cells of the embryonic foregut may account for the presence of pancreatic tissue in the stomach, Meckel's diverticulum, and intestinal duplications. Usually asymptomatic ectopic pancreatic tissue in the intestine is increasingly recognized as a potential source of pyloric obstruction, disruption of

Omentum Mesentery

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Figure 4. Heterotopic pancreas. Relative frequency is indicated by width of arrows. The most frequent sites are the stomach and duodenum. (From Gray SW, Skandalakis JE: Embryology for Surgeons. Philadelphia, WB Saunders, 1972, p 269.)

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normal peristalsis, production of peptic ulcer, or neoplasm. Ravitch49 believes that the presence of an ulcerated nodule of ectopic pancreas in the stomach or duodenum may give rise to ulcer-like symptoms that are relieved by removal of the nodule.

Pancreatic Gallbladder

Boyden,S in 1926, described gallbladder duplications in cats in which the accessory organ arose from the ventral pancreatic bud instead of from the cystic primordium. He suggested that some duplications in humans might be of this type. Wrenn and Favara,67 confirmed by Boyden,u reported the presence of a human pancreatic gallbladder. Pancreatic tissue in the wall of an otherwise normal gallbladder,31 however, does not indicate origin from the ventral pancreatic primordium.34

PANCREAS DIVISUM-MYTH OR REALITY?

Failure of the dorsal and ventral pancreatic part to fuse may result in separate draining of the ducts of Wirsung and Santorini. With endoscopic retrograde cholangiopancreatography (ERCP) in asymptomatic points the incidence is approximately 5%. Perhaps 25% of these will develop pancreatitis, maybe secondary to stenosis or obstruction of one or both ducts. Is the pancreas divisum a myth? We do not know. Sphincteroplasty on both ducts and cholecystectomy to avoid stones is the procedure of choice at the present time.

RELATIONSHIP OF THE PANCREAS TO ADJACENT ORGANS

No other organ in the human body is surrounded so closely by so many other anatomic entities as is the pancreas. Because of this, pancreatic cancer can and often does invade the duodenum, stomach, spleen, left adrenal, transverse colon, left kidney, jejunum, and right ureter. 1S An appreciation of the anterior and posterior relations may be gained by viewing Figures 5 to 7.

PARTS OF THE PANCREAS Head

The head of the pancreas is flattened and has an anterior and posterior surface. The anterior surface is adjacent to the pylorus and the

Figure 5. Anterior relationships. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Ana· tomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

Figure 6. Bare areas of the duo· denum. The pancreas is in inti· mate contact with the duodenum along the concave surface. The attachment of the transverse mesocolon produces an additional bare area. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Ana· tomical complications of pan· creatic surgery. Contemporary Surgery 15:17-50, 1979; with per· mission.)

Transverse' mesocolon bare area

Vena cava

Figure 7. Posterior relationships. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

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transverse colon. The anterior pancreaticoduodenal arcade parallels the duodenal curvature and is related to the pancreatic surface. The posterior surface is close to the hilus and medial border of the right kidney, the right renal vessels and the inferior vena cava, the right crus of the diaphragm, the posterior pancreaticoduodenal arcade, and the right gonadal vein. The distal portion of the common bile duct may lie behind the pancreatic head in a groove (15%), or it may be partially or totally embedded in the pancreatic substance (85%).2 Common Bile Duct

The relation of the head and common bile duct (Fig. 8) is as follows: Embryologically, anatomically, and surgically, the distal common bile

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Figure 8. Five variations of the relation of the third part of the common bile duct to the pancreas. The bile duct is partially covered by a tongue of pancreatic tissue in 44% of cases (A and B), it is completely covered in 30% (e), uncovered on the posterior surface of the pancreas in 16.5% (0), and covered by two tongues of pancreas in 9% (E). (From Gray SW, Skandalakis JE: Embryology for Surgeons. Philadelphia, WB Saunders, 1972, p 243.)

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duct, the duodenum, and the pancreas form an inseparable unit. Osler poetically described this as the abdominal area of romance, "where the head of the pancreas lies folded in the arms of the duodenum."14 Their relations and blood supply make it impossible for the surgeon to remove completely the head of the pancreas without removing the duodenum and the distal part of the common bile duct. The common bile duct is located to the right of the gastroduodenal artery, at the posterior wall of the first portion of the duodenum. Frequently, this artery crosses the supraduodenal portion of the common bile duct anteriorly or posteriorly. The posterior superior pancreaticoduodenal artery "double crosses" the third portion of the common bile duct, first passing ventral to the duct at the point of the origin from the agastroduodenal artery, and second passing dorsal to the duct a few millimeters above the entrance of the duct into the duodenum. Intubation of the common bile duct is a wise step. This is due to the possibility of variations in the topographic anatomy of the distal common bile duct in relation to the head of the pancreas as well as to each relation with vessels. Uncinate Process

The uncinate process (Fig. 9) is a small hook-like prolongation of pancreatic tissue of variable size, shape, extension, and weight originat-

Figure 9. Variations in the extent of the uncinate process of the pancreas. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

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ing from the left lower part of the head with upward and to the left projection-in most cases, behind to the small vessels and in front of the aorta. Dissection of the uncinate process in 20 fresh cadavers resulted in 18 with uncinate process and two without. Therefore, in most cases it lies between the inferior vena cava and the aorta and covers the superior mesenteric vessels superiorly and ventrally. The presence or absence of the uncinate process dictates how much of the pancreas is removed. A well-developed uncinate process most likely belongs to a pancreas with a small head. We therefore agree with Fry and Child30 that if the uncinate process is present, then a 60% to 65% pancreatectomy is done; if the uncinate process is absent, 70% to 80% of the pancreas is removed. Remember the following points: 1. The extent of resection is empiric. 2. Division at the neck equals 60% to 70% resection. 3. Division at the proximal body to the left of the portal vein above and to the superior mesenteric vein below is 50% to 60%. 4. With 80% pancreatectomy there is good exocrine and endocrine activity. 5. We do not know about the normal physiology of the in situ remaining pancreas because we do not know how much pancreatic disease is present. Does the pancreatic segment have enough islet cells? 6. Our effort to weigh proximal and distal pancreas with or without uncinate process in 20 subjects did not give any satisfactory answers. The Ligament of the Uncinate Process

We have seen the ligament in cases in which the uncinate process ends at the vicinity of the superior mesenteric vein. If such is the case, the ligament is quite dense and it fixes the process to the superior mesenteric artery. Pancreatitis or cancer makes the fixation more concrete. An anomalous hepatic artery may pass through the uncinate process. Because the aorta is behind the uncinate process, pancreatic carcinoma can be heavily fixed with the aorta. Neck

The neck of the pancreas (Fig. 10) is 1.5 to 2.0 cm long. It is covered partly anteriorly by the pylorus and extends to the right as far as the origin of the anterosuperior pancreaticoduodenal artery from the gastroduodenal artery; the left boundary of the neck is arbitrary. Posterior to the neck, the portal vein is formed by the confluence of the superior mesenteric and splenic veins. There are usually no anterior pancreatic tributaries to these veins, but occasionally a few short veins may exist.

SURGICAL EMBRYOLOGY AND ANATOMY OF THE PANCREAS

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vein

H~=-- Uncinate process

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of pancreas portion of duodenum

Transverse colon Small intestine

Figure 10. Sagittal section through the neck of the pancreas. The uncinate process and the third part of the duodenum lie posterior to the superior mesenteric artery (SMA). The midline colic artery (MeA) leaves the SMA at the inferior pancreatic margin to travel in the transverse mesocolon. (From Akin JT, Gray SW, Skandalakis JE: Vascular compression of the duodenum: Presentation of ten cases and review of the literature. Surgery 79(5):515, 1976; with permission.)

Careful elevation of the neck and ligation of such vessels, if present, may be necessary. Otherwise, bleeding may make it difficult to evaluate the structures lying beneath the neck. From the right, the portal vein receives a few short vessels; from the left, the portal vein receives the left gastric, the splenic, and sometimes the inferior mesenteric veins. Body

The anterior surface of the body of the pancreas is covered by the double layer of peritoneum of the omental bursa that separates stomach from pancreas. It also is related to the transverse mesocolon, which divides into two leaves, the superior covering the anterior surface, and the inferior passing inferior to the pancreas. The middle colic artery emerges from beneath the pancreas to travel between the leaves of the mesocolon. Posteriorly, the body is related to the aorta, the origin of the superior mesenteric artery, the left crus of the diaphragm, the left kidney and its vessels, the left adrenal gland, and the splenic vein. Small vessels from the pancreas enter this vein. These must be ligated during pancreatectomy if the splenic vein and the spleen are to be preserved.

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Tail

The tail of the pancreas is relatively mobile; its tip in most cases (Fig. 11) reaches the hilus of the spleen. Together with the splenic artery and the origin of the splenic vein, it is contained between two layers of the splenorenal ligament. The outer layer of this ligament is the posterior layer of the gastrosplenic ligament. Careless division may injure the short gastric vessels. The ligament is almost avascular, but digital manipulation should stop at the pedicle. Busnardo et al13 divide the pancreas into two anatomicosurgical segments suitable for transplantation. Thirty corrosion pancreatic specimens showed right (cephalocervical) and left (corporocaudate) segments. These are separated by a paucivascular area.

THE PANCREATIC DUCTS Anatomy and Variations

The main pancreatic duct (of Wirsung) arises in the tail of the pancreas. Through the tail and body of the pancreas, the duct lies midway between the superior and inferior margins and slightly more posterior than anterior. The main pancreatic duct and the accessory duct lie anterior to the major pancreatic vessels. The main duct crosses the vertebral column between the 12th thoracic and the second lumbar vertebrae. Is. s4 In more than one half of persons, the crossing is at the first lumbar vertebra. 60 In the tail and body of the pancreas, from 15 to 20 short tributaries enter the duct at right angles. I Superior and inferior tributaries tend to alternate. In addition, the main duct may receive a tributary draining the uncinate process. In some individuals, the accessory pancreatic duct empties into the main duct. Small tributary ducts in the head may open directly into the intrapancreatic portion of the common bile duct. 32 The main duct turns caudad and posterior on reaching the head of the pancreas. At the level of the major papilla, the duct turns horizontally to join the caudal surface of the common bile duct. It then enters the wall of the duodenum, usually at the level of the second lumbar vertebra. The accessory pancreatic duct (of Santorini) may drain the antero-

Figure 11. Relations of the tail of the pancreas to the splenic portas. (From Skandalakis JE, Colborn GL, Pemberton LB, et al: The surgical anatomy of the spleen. Problems in General Surgery 7:1, 1990; with permission.)

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superior portion of the head, either into the duodenum at the minor papilla or into the main pancreatic duct (Fig. 12). Frey29 reports, "The main pancreatic duct in the body and tail of the pancreas arising from the dorsal bud lies in a horizontal plane. On the other hand, the main duct of Wirsung in the head of the pancreas arising from the ventral bud passes in almost an anteroposterior plane." Frey further states that if the head is 5 cm thick and the distance is 3 cm from the duodenum to the junction of the main pancreatic duct at which the duct courses posteriorly and inferiorly, the distance from the junction of the central and dorsal duct to the ampulla of Vater is 6 cm. He believes that the major pancreatic duct in the head may not be drained well by filleting this portion of the surface of the gland. Because of the developmental origin of the two pancreatic ducts, a number of variations are encountered; most can be considered normal. The usual configuration is seen in Figures 13A and 14A. Smaller than the main pancreatic duct (of Wirsung), the accessory duct (of Santorini) opens into the duodenum on the minor papilla. Configurations 13B to E show examples of progressive diminution in size of the accessory duct. Figures 14A to 0, starting from the usual configuration, A, are examples of prominence of the accessory duct and lessening caliber of the main duct. Type A is the most common. In about 10% of individuals, there is no connection between the accessory duct and the main duct-'3 (see Figs. 130 and 14C and 0). It is important to remember this when contrast medium is injected into the main duct. There is no minor papilla in 30% (see Fig. 13B, C, and E). In some individuals with a minor papilla, the terminal portion of the accessory duct is too small to permit the passage of any quantity of fluid. Three papillae have been seen4,so (Fig. 15A and 0). A curious loop in the main pancreatic duct (Fig. 15B) was found in 3 of 76 specimens examined by Baldwin2; an identical example was reported by Rienhoff and Pick':' rell. so Length, Width, and Capacity

The greatest diameter of the main pancreatic duct is in the head of the pancreas, just before the duct enters the duodenal wall (Fig. 16). This Dorsal Pancreatic Anlage

Figure 12. A highly diagrammatic representation of the embryogenesis of the proximal and distal pancreatic ducts. S = duct of Santorini; W = duct of Wirsung; M = main pancreatic duct.

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Figure 13. Variations of the pancreatic duct. Degrees of suppression of the accessory duct: A, Both ducts open into the duodenum in 60% of cases; B, the accessory duct ends blindly in the duodenal wall; C, the accessory duct ends blindly before reaching the duodenum in 30% of cases; D, the accessory duct has no connection with the main duct; and E, the accessory duct is absent. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

ranges from 3.1 to 4.8 mm. The duct gradually tapers toward the tail to a diameter ranging from 0.9 to 2.4 mm. Like the bile duct, the pancreatic duct is constricted in the wall of the duodenum. Kasugai et aP8 found that 2 to 3 mL of contrast medium will fill the main pancreatic duct in the living patient; 7 to 10 mL will fill the branches and the smaller ducts. Trapnell and Howard58 found 0.5 to 1.0 mL sufficient to fill the duct system in autopsy specimens. THE MAJOR DUODENAL PAPILLA

Although this structure bears the name of Abraham Vater,61 it was illustrated first by Bidloo of The Hague in 1685.6

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VI

Figure 14. Degrees of suppression of the main duct: A, Both ducts open into the duodenum; B, the main duct is smaller than the accessory duct; C, the main duct has no connection with the larger accessory duct present in 10% of cases; and 0, the main duct is short or absent in 10% of cases. The accessory duct drains almost the whole pancreas. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

The papilla is on the posteromedial wall of the second portion of the duodenum, 7 to 10 cm from the pylorus.66 Rarely, the papilla may be in the third portion of the duodenum. On endoscopy, the papilla has been reported to lie to the right of the vertebral column at the level of the second lumbar vertebra in 75%60 to 85%17 of bodies examined. Kreel and Sandin39 found it to lie at the level of the third lumbar vertebra in 57% of autopsy specimens. Viewed from the mucosal surface of the duodenum, the papilla is located where a longitudinal mucosal fold or frenulum meets a transverse mucosal fold to form a T (Fig. 17). The papilla may not be obvious because too much traction erases the folds, or it may be covered by one of the transverse folds. At the operation, if the T is not apparent and the papilla cannot be palpated, the common bile duct must be probed from above. A duodenal diverticulum close to the papilla may confuse the surgeon or the endoscopist. THE AMPULLA (OF VATER)

The ampulla is a dilatation of the common pancreatobiliary channel adjacent to the papilla and below the junction of the two ducts (Fig. 18A).

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~ ~ Figure 15. Variation of the pancreatic ducts. Rare forms: A, duplication of the accessory duct; B, loop in the main duct; C, anomalous course of accessory duct; and 0, triple pancreatic ducts. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50,1979; with permission.)

If a septum is present as far as the duodenal orifice, no ampulla exists (Fig. 18B and C). Michels46 collected the findings of 25 investigators in 2500 specimens and concluded that an ampulla was present in 64%. An ampulla was said to be present if the edge of the septum between the two ducts did not reach the tip of the papilla. Actual measurements of the distance between septal edge and papillary tip range from 1 to 14 mm, 75% being 5 mm or less. 50 The following classification of Michels is the most useful: Type 1: The pancreatic duct opens into the common bile duct at a variable distance from the opening in the major duodenal papilla (Fig. 18A and B). The common channel mayor may not be dilated (85%). Type 2: The pancreatic and bile ducts open close to one another, but separately, on the major duodenal papilla (5%) (Fig. 18C). Type 3: The pancreatic and bile ducts open into the duodenum at separate points (9%). A true ampulla with dilatation is present in about 75% of individuals of type 1 and is absent in types 2 and 3. THE SPHINCTER OF BOYDEN

Several sphincters of smooth-muscle fibers surround the intramural part of the common bile duct, the main pancreatic duct, and the ampulla,

SURGICAL EMBRYOLOGY AND ANATOMY OF THE PANCREAS

HEAD

BODY 1---+---1

Classen et al. (1973L ____ A.8 mm Kasugai et al. (1972L ___ 2.6 - 3.5 *Kreel & Sandin (1973I...J.2 - 5.3 *Millbourn (1960) (age 16 - 5O!.. __ ___ 3.76 (age 51 - 921. _____ .4. 73 Nebel & Fornes (1973L ___ J.3 Ogoshi et al. (1973L ______ 3.4 Oi 119721. _______________ 3.6 Sivak & Sullivan (1976L __ 3. 2 Varley et al. (1976L _____ 3.1 * autopsy specimens

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_____ 2.'4 mm ___ 1.0-1.7 ___ 1.4 - 2.1

_____ 2.9 _____ 2.7 _____ 2.3 ____ 2.0

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Figure 16. Diameter of the main pancreatic duct in the head, body, and tail as reported by several authors. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15: 17-50, 1979; with permission.)

if present (Fig. 19). The complex has a separate embryonic origin from

that of the duodenal musculature and is functionally separate. Although the anatomy has been well described by Boyden9, 10 and others, the terminology is unsettled. We would call the entire sphincter complex the "sphincter of Boyden" in recognition of his contribution to the anatomy of this region. The total length of the complex may range from 6 to 30 mm, depending upon the obliquity of the path taken by the biliary and pancreatic ducts through the duodenal wall. In some instances, the sphincter may extend beyond the duodenal wall into the pancreatic portion of the bile duct. 64 It is important to be aware of this fact when sphincterotomy is done.

THE MINOR DUODENAL PAPILLA

The minor duodenal papilla is situated about 2 cm cranial and slightly anterior to the major papilla. It is smaller and its site does not have the characteristic mucosal folds that mark the site of the major papilla. Baldwin2 found the minor papilla to be present in all of a series of 100 specimens. In a sample of the same size, however, Dowdy and

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Figure 17. The T arrangement of duodenal mucosal folds, indicating the site of the major duodenal papilla. A mucosal fold may cover the orifice of the papilla in some cases. No such arrangement marks the site of the minor papilla. The major papilla is rarely this obvious. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50,1979; with permission.)

Figure 18. Variations in the relation of the common bile duct and main pancreatic duct at the duodenal papilla. A, Minimal absorption of the ducts into the duodenal wall during embryonic development; an ampulla is present. e, Partial absorption of the common channel; no true ampulla is present. C, Maximum absorption of the ducts into the duodenum. Separate orifices on the papilla, no ampulla. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

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Figure 19. The four sphincters making up the sphincter of Boyden: (1) superior choledochal sphincter, (2) inferior choledochal sphincter, (3) sphincter ampullae (papillae), and (4) sphincter pancreaticus. The measurements are those of White (1973). (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

associates25 could find no minor papilla in 18 specimens. It may be noted, however, that some papillae may be difficult to identify. An excellent landmark is the gastroduodenal artery, situated anterior to the accessory pancreatic duct (Santorini) and the minor papilla. During gastrectomy, duodenal dissection should end proximal to or at this artery. It becomes especially important in the few patients in whom the accessory duct carries the major drainage of the pancreas. VASCULAR SUPPLY OF THE PANCREAS Arterial Supply

Blood is supplied to the pancreas from both the celiac trunk and the superior mesenteric artery (Figs. 20 and 21). Variations are common, and differing textbook illustrations are all "correct" for at least some patients. The head of the pancreas and the concave surface of the duodenum are supplied by two pancreaticoduodenal arterial arcades. These are always present. They are formed by a pair (anterior and posterior) of superior arteries from the celiac trunk that join a second pair of inferior arteries from the superior mesenteric artery. These vascular arcades are the chief obstacles to complete pancreatectomy without duodenectomy. Ligation of both vessels results in duodenal ischemia and necrosis. At the neck, the dorsal pancreatic artery usually arises from the splenic artery, close to its origin from the celiac trunk. A right branch supplies the head of the pancreas and usually joins the posterior arcade. One or two left branches pass through the body and tail of the pancreas, often making connections with branches of the splenic artery and, at the tip of the tail, with the splenic or the left gastroepiploic artery. All major arteries lie posterior to the ducts.

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Gastroauodenol a

Ant

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Inf pancreaticoduodenal a

Figure 20. Anterior view of the major arterial supply to the pancreas; left and right gastric arteries are not shown. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

The Pancreatic Arcades

The gastroduodenal artery arises as the first major branch of the common hepatic branch of the celiac trunk. About 1 cm from its origin, it gives off the right gastroepiploic artery. It subsequently divides to

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Sup.

,/

mesenteric o.

Figure 21. Posterior view of the major arterial supply to the pancreas; left and right gastric arteries are not shown. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

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form the anterior and posterior superior pancreaticoduodenal arteries. All three branches occasionally may arise by trifurcation of the gastroduodenal artery. The anterosuperior pancreaticoduodenal artery lies on the surface of the pancreas. It provides 8 to 10 branches to the anterior surface of the duodenum, one to three branches to the proximal jejunum, and numerous branches to the pancreas. During pancreatic resection, the duodenal branches can be sacrificed, but the jejunal branches should be preserved. The artery enters the substance of the pancreas. On the posterior surface, it joins the anteroinferior pancreaticoduodenal artery from the superior mesenteric artery. Melliere42 found four instances in which the anastomosis between superior and inferior vessels appeared narrow or absent, but he believed this to be the result of transitory spasm. The anteroinferior pancreaticoduodenal artery arises from the superior mesenteric artery at, or above, the inferior margin of the pancreatic neck. It may form a common trunk with the posteroinferior artery. One or both vessels may arise from the first or second jejunal branches of the superior mesenteric artery. Ligation of the jejunal branch endangers the blood supply to the fourth part of the duodenum. Even more striking are instances in which a posteroinferior artery arises from an aberrant right hepatic artery springing from the superior mesenteric artery. The posterosuperior pancreaticoduodenal artery arises from the gastroduodenal artery. Its course is visible only when the posterior surface of the pancreas is exposed (see Fig. 21). Branches may anastomose with branches of the gastroduodenal artery or with a right branch of the dorsal pancreatic artery. Other branches supply the anterior and posterior surfaces of the first part of the duodenum. The course of the posterior arcade is further from the duodenum than is that of the anterior arcade. It passes posterior to the intrapancreatic portion of the common bile duct. The posterior arcade, like the anterior, may be doubled or tripled, the extra arcades joins the posteroinferior pancreaticoduodenal artery, or the superior mesenteric artery. The posterior arcade also may anastomose with an aberrant right hepatic artery from the superior mesenteric artery (Fig. 22C), either separately or together with the anterior arcade. Michels46 has provided an exhaustive description of the possible variations that may be encountered. The Branches of the Splenic Artery

The splenic artery on the posterior surface of the body and tail of the pancreas loops above and below the superior margin of the organ. It becomes more tortuous with increasing age of the person. The first major branch is the dorsal pancreatic artery, which usually joins one of the posterosuperior arcades after giving off the inferior (transverse) pancreatic artery to the left. The origin of the latter artery is variable; it may be doubled or absent. It mayor may not freely anastomose with the splenic artery in the body and tail of the pancreas. If there are no anas-

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Figure 22. Variations of the hepatic arteries. A, The normal configuration in which the common hepatic artery arises from the celiac trunk. B, An anomalous common hepatic artery arises from the superior mesenteric artery. C, An anomalous right hepatic artery arises from the superior mesenteric artery. D, An anomalous left hepatic artery arises from the superior mesenteric artery. E, An anomalous left hepatic artery arises from the gastroduodenal artery. The anomalous artery may be accessory to, or replacing, a normal hepatic artery. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

tomoses, thrombosis of the inferior pancreatic artery may produce infarction and necrosis. Ligation of the splenic artery does not require splenectomy; ligation of the splenic vein does. The Caudal Pancreatic Artery

The caudal pancreatic artery arises from the left gastroepiploic artery or from a splenic branch at the hilus of the spleen. It anastomoses with branches of the great pancreatic and other pancreatic arteries. The caudal pancreatic artery supplies blood to accessory splenic tissue when it is present at the hilus.

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Anomalous Hepatic Arteries

The common hepatic artery is usually a main branch of the celiac trunk, which arises cranial to the pancreas (Fig. 22A). The surgeon must always look for a possible anomalous hepatic artery before proceeding with a pancreatic resection. An anomalous common hepatic artery arises from the superior mesenteric artery in from 2.0% to 4.5% of persons.45 ,57 It is related to the head or neck of the pancreas and occasionally passes through the head (Fig. 22B). It subsequently passes behind the portal vein, and almost the entire blood supply of the duodenum comes from the superior mesenteric artery. Accidental ligation of this vessel not only results in hepatic ischemia and perhaps necrosis but also jeopardizes the duodenum. Selective arteriography before an elective pancreatic operation is of great assistance in the operating room. An anomalous right hepatic artery is more frequent. It arises from the superior mesenteric artery. Although its course is unpredictable, it is related to the head and neck of the pancreas. Such an artery may pass behind the common bile duct or the portal vein (Fig. 22C). An aberrant right hepatic artery was present in 26% in Michels' series. 45 It may give off the inferior pancreaticoduodenal arteries. An anomalous left hepatic artery presents a problem 'in operations on the pancreas only when it arises from the right side of the superior mesenteric artery (Fig. 22D) or from the gastroduodenal artery (Fig. 22E). Michels found an anomalous left hepatic artery in 27% of his specimens. Anomalous Middle Colic Artery

A middle colic artery may pass through the head of the pancreas or between the head and the duodenum. It may arise from the superior mesenteric, the dorsal pancreatic, or the inferior pancreaticoduodenal arteries.

Venous Drainage

In general, the veins of the pancreas parallel the arteries and lie superficial to them. Both lie posterior to the ducts. The drainage is to the portal vein, the splenic vein, and the superior and inferior mesenteric veins (Figs. 23 and 24). Surgical note: Triller and Schweize~2 advised angiography prior to surgery. Donatini23 notes that selective arteriography and phlebography will help the surgeon make the right decision of limited surgery. Such will help to ensure that the remaining pancreas has a good blood supply. Further, we disagree with the majority opinion of the panel of the World Congress of Surgeons, which discussed "Controversies in the Management of Pancreatic Cancer" in August of 1992, in Stockholm and advised that arteriography is not necessary prior to pancreatic surgery.

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a

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Figure 23. Anterior view of the venous drainage of the pancreas. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50,1979; with permission.)

The anomalies and variations are too many for the surgeon to navigate in uncharted waters.

Venous Supply

Veins of the Head of the Pancreas

Four pancreaticoduodenal veins form venous arcades that drain the head of the pancreas and the duodenum. The anterosuperior pancreaticoduodenal vein joins the right gastroepiploic vein. This vein receives a colic vein to form a short gastrocolic vein, which is a tributary to the superior mesenteric vein. The posterosuperior vein enters the portal vein above the superior margin of the pancreas. The anterior and posterior inferior pancreaticoduodenal veins enter the superior mesenteric artery together or separately. Other small, unnamed veins in the head and neck drain independently into the superior mesenteric vein and the right side of the portal vein. 27 The surgeon must avoid traction of the head and ligate these veins carefully. White64 states that pancreatic tributaries do not enter the anterior surface of the portal or superior mesenteric veins. As a result, the risk of bleeding when incising the neck of the pancreas is reduced. Silen,53 however, warns that in some patients the superior pancreaticoduodenal vein and the gastrocolic vein may enter the portal vein and the superior mesenteric vein anteriorly.

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Portal v.

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Figure 24. Posterior view of the venous drainage of the pancreas and formation of the hepatic portal vein. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

Veins of the Neck, Body, and Tail of the Pancreas

The veins of the left side of the pancreas form two large venous channels, the splenic vein above and the transverse (inferior) pancreatic vein below. A smaller superior pancreatic vein may sometimes be identified. The splenic vein receives from 3 to 13 short pancreatic tributaries. 24 In a few instances one such tributary entered the left gastroepiploic vein in the tail of the pancreas. The inferior mesenteric vein terminates in the splenic vein in about 38% of individuals, and the left gastric vein has a similar ending in 17%. The inferior pancreatic vein may enter the left side of the superior mesenteric vein, the inferior mesenteric vein, or occasionally the splenic or the gastrocolic veins. The Portal Vein

The hepatic portal vein forms behind the neck of the pancreas by the union of the superior mesenteric and splenic veins (see Fig. 24). The inferior mesenteric vein entered at this junction in about one third of specimens examined by Douglass and associates. 24 In another third, the inferior mesenteric joined the splenic vein close to the junction. In the remainder, it joined the superior mesenteric vein. The portal vein lies behind the pancreas and in front of the inferior vena cava, with the common bile duct to the right and the hepatic artery to the left. The portal vein and the superior mesenteric vein can be separated easily from the posterior surface of the pancreas in the absence of disease. In 23 cadavers we dissected, the left gastric (coronary) vein entered

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the portal vein in 17 and the splenic vein in 6. When drainage was to the portal vein, the left gastric vein lay in the gastrohepatic ligament. Rarely, the portal vein may lie anterior to the pancreas and the duodenum and represents persistence of the preduodenal rather than the postduodenal plexus of the embryonic vitelline veins. Inadvertent section of this vessel could be fatal. It is often associated with annular pancreas, malrotation, and biliary tract anomalies (Fig. 25).

LYMPHATIC DRAINAGE OF THE PANCREAS

As might be expected from the position of the pancreas, lymphatic drainage is centrifugal to the central groups of nodes. No standard terminology for those nodes exists, although Evans and Ochsner6 have proposed one. None of the efforts to demarcate specific drainage areas of the pancreas have gained wide acceptance. 26, 36, 51 Studies of Cubilla et aps have provided the basis from most recent works. The lymphatic vessels of the pancreas arise in a rich, perilobular, inter anastomosing network. This is followed by channels coursing along the surface of the gland and in the interlobular spaces with the blood vessels. These lymphatics drain into five main collecting trunks and lymph node groups (Fig. 26).

-·Inf mesenteric v.

A

Figure 25. Some rare anomalies of the portal vein. A, The portal vein lies anterior to the duodenum. B, The pulmonary veins drain anomalously into the portal vein. This is one form of total anomalous pulmonary drainage. It may be associated with severe cardiac defects. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

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Figure 26. Distribution of lymph nodes in 18 pancreatectomy resection specimens. Numerator of fraction of each group indicates number of patients with metastasis in that lymph node group; denominator indicates number of patients in which group nodes were examined. Thirteen cases were pancreas duct cancer, five were other cancers in the head of the pancreas area. SH = superior head; SB = superior body; IH = inferior head; IB = inferior body; APD = anterior pancreaticoduodenal; PPD = posterior pancreaticoduodenal; CBD = common bile duct; Py = pyloric; LC = lesser curvature; GC = greater curvature; S = tail of pancreas and splenic; JE = jejunal; Col = mid colic. (From Cubilla AL, Fortner J, Fitzgerald PJ: Lymph node involvement in carcinoma of the head of the pancreas area. Cancer 41 :880, 1978; with permission.)

Superior Nodes

The collecting trunks of this group of nodes arise from the anterior and posterior upper half of the pancreas. Most of them end in the suprapancreatic lymph nodes located along the superior border of the pancreas. Designation may follow respected area, superior head and superior body. Some lymphatics occasionally terminate in the nodes of the gastropancreatic fold or in the lymph nodes of the hepatic chain. Inferior Nodes

These collecting trunks drain the anterior and posterior lower halves of the head and body of the pancreas. They lead into the inferior pancreatic group of lymph nodes, most located along the inferior border of the head and body of the pancreas. Further, they may extend into the superior mesenteric and left lateroaortic lymph nodes. Although infrequent, a collecting trunk may terminate directly in a lumbar trunk. Anterior Nodes

Two collecting trunks run along the anterior surface of both superior and inferior portions of the head of the pancreas. They extend to the

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infrapyloric and the anterior pancreaticoduodenal lymph nodes. They also may extend to some of the mesenteric lymph nodes at the root of the mesentery of the transverse colon. Posterior Nodes

These follow the posterior surface of the superior and inferior portions of the head of the pancreas. They drain into the posterior pancreaticoduodenal lymph nodes, the common bile duct lymph nodes, the right lateroaortic lymph nodes, and to some nodes at the origin of the superior mesenteric artery. Most of the lymphatics of the common bile duct and ampulla of Vater also end in the posterior pancreaticoduodenal group of lymph nodes . Splenic Nodes

These lymphatics lead from the tail of the pancreas. They drain into the following lymph nodes: those at the hilum of the spleen, phrenolienal ligament, and at the inferior and superior lymph nodes of the tail of the pancreas. A few lymphatic channels, however, end in the lymph nodes superior and inferior to the body of the pancreas. No lymphatic communications exist between the pancreas and the lymph nodes of the greater and lesser curvatures of the stomach. The lymphatics of the head and body of the pancreas do not drain into the tail of the pancreas or the splenic nodes. Rarely, however, the lymph vessels from the tail of the pancreas can terminate in the superior body and inferior body subgroups of nodes. Examination of surgical specimens removed during regional pancreatectomy in patients with pancreatic and peripancreatic cancers revealed both the number of lymph nodes present in each of the nodal drainage areas as well as the presence of metastatic disease in them. IS The average number of lymph nodes present in each lymph node group was as follows: (1) superior nodes: 17 superior head, 13 superior body; (2) inferior group: one inferior body, one midcolic, no inferior head; (3) anterior group: three pancreaticoduodenal, three jejunal mesenteric. We continue to learn more about the pancreatic lymphatics. Deki and Sato22 stated that the lymphatics of the anterior surface of the head of the pancreas and the neck are associated with the common hepatic group and with the superior mesenteric nodal group, all terminating in the node at the right of the origins of the celiac trunk and the superior mesenteric artery. Lymphatics of the posterior surface of the head terminate in a node that is located behind the previously described node. The lymphatics of the left half of the pancreas terminate in a node to the left of the celiac trunk and superior mesenteric artery. Both the right and left nodes drain into the abdominal aortic nodes.

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Pissas48 questions the value of radical surgery, perhaps owing to very rapid passage of lymph into the thoracic duct. Donatini and HiddenZ 3 studied the routes of lymphatic drainage from the pancreas by dissection and injection to several pancreatic segments. They concluded that injection of dye in the body and tail followed the splenic and inferior pancreatic pathways with termination at first to the left interceliomesenteric node and then to the supra- and infrarenal lymph nodes. From the head of the pancreas, dye followed three routes: (1) The lymphatics of the anterior and posterior aspects of the head follow the superior mesenteric route and reach the right interceliomesenteric node and then terminate bilaterally to the supra- and infrarenal nodes; (2) The anterosuperior segment of the head follows two routes: the gastroduodenal joining the right interceliomesenteric node and an inferior route that terminates by backward direction to the isthmus; (3) The posterosuperior segment of the head follows the common bile duct and hepatic artery, reaching the pericholedochal nodes and hepatic pedicular nodes and occasionally the right interceliomesenteric node. These authors consider the right interceliomesenteric node the principal relay station for the head of the pancreas.

THE NERVE SUPPLY OF THE PANCREAS Innervation of the pancreas occurs by the sympathetic division of the autonomic nervous system by way of the splanchnic nerves, and by the parasympathetic division by way of the vagus nerve. These nerves generally follow blood vessels to their destination. Efferent (motor) fibers to the wall of the blood vessels, the pancreatic duct, and pancreatic acini are contained by both divisions. Further, both contain visceral afferent (pain) fibers. The distribution of these, however, is not well understood in the pancreas (Fig. 27). Sympathetic innervation is from the greater splanchnic nerve and the lesser splanchnic nerve. The former is composed of preganglionic efferent fibers from the fifth to the ninth or tenth thoracic segments. The latter is composed of fibers from the ninth and tenth or the tenth and eleventh segments. Some fibers may be contributed by the least splanchnic nerve. These nerves pierce the diaphragmatic crura to enter the celiac plexus and the celiac ganglion. They pass through these to reach the pancreas. Some afferent fibers cross the midline in the plexus? The celiac ganglion contains cell bodies of efferent fibers to the pancreas. Cell bodies of afferent fibers are in the dorsal root ganglion, where they may have connections with somatic sensory fibers. Parasympathetic innervation is by way of the celiac division of the posterior vagus trunk. The afferent fibers are preganglionic from cell bodies in the brain. Efferent fibers are dendrites of cell bodies in the brain. Vagal fibers pass through the esophageal hiatus of the diaphragm, usually as anterior and posterior trunks. The posterior trunk divides into

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Figure 27. The autonomic nerve supply to the pancreas. (From Skandalakis JE, Gray SW, Rowe JS Jr, et al: Anatomical complications of pancreatic surgery. Contemporary Surgery 15:17-50, 1979; with permission.)

.. Sup mesenteric ganglion

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Figure 28. Sagittal section through the abdomen. Anterior pararenal space (striped); perirenal space (stipp/ed); posterior pararenal space (crosshatched). (From Meyers MA: Dynamic Radiology of the Abdomen. New York, Springer-Verlag, 1976, p 118; with permission.)

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a posterior gastric and a celiac division near the lesser curvature of the stomach.55 The latter division enters the celiac plexus, which supplies vagal branches to the lower abdominal viscera. Neither afferent nor efferent fibers synapse in the celiac ganglion.

THE EXTRAPERITONEAL SPACES AND THE PANCREAS

The posterior parietal peritoneum and the transversalis fascia are the anterior and posterior bounds of the retroperitoneal space, respectively. This space extends from the pelvic brim inferiorly to the diaphragm superiorly. Among the major structures it encompasses are the adrenal glands, the kidneys, the ureters, portions of the duodenum, the pancreas, the inferior vena cava, the aorta, the portal vein, and the ascending and descending colon. In a horizontal cross-section, it is somewhat C-shaped owing to the curvature of the lumbar spine. As a result, some retroperitoneal structures (the pancreas and duodenal loop) lie anterior to others (the spleen, kidneys, and posterior aspect of the liver). Meyers43 divided the extraperitoneal region into three compartments according to their demarcation by well-defined fascial planes. The anterior and posterior layers of Gerota's fascia are central to the division of the extraperitoneal region. The kidney and the perirenal fat are enveloped by this dense sheath. The fusion of its two layers behind the ascending or descending colon forms a single lateroconal fascia. This continues around the flank to blend with the peritoneal reflection to form the pericolic gutter (Figs. 28B and 29). Meyers named these three compartments: (1) the anterior pararenal space. This extends from the posterior parietal peritoneum to the anterior renal fascia, and is confined laterally by the lateroconal fascia (Figs. 28A, 29); (2) the perirenal space. This is the space in which the kidney and perirenal fat reside within the confines of Gerota's fascia (Figs. 28 to 30); (3) the posterior pararenal space. This extends from the posterior renal fascia to the transversalis fascia. It is a thin layer of fat lateral to the lateroconal fascia, also known as the "preperitoneal fat" (see Figs. 28 to 30). The extraperitoneal portions of the alimentary tract, the ascending and descending colon, the duodenal loop, and the pancreas are included within the anterior pararenal space. This space is continuous across the midline (the striped areas in Figure 27A). It is important to understand this anatomy when considering the pathways that pancreatic extravasations can take. The perirenal spaces have no continuity across the midline. This is due to the fusion of the posterior fascial layers with the psoas or quadratus lumborum fascia medially, and to the fusion of the renal fascia with the dense mass of connective tissue surrounding the great vessels in the root of the mesentery and behind the pancreas and duodenum anteriorly.

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Figure 29. The three extraperitoneal spaces: (1) the anterior pararenal space, (2) the perirenal space, and (3) the posterior pararenal space. C = colon; K = kidney; PM = psoas major muscle. (From Meyers MA: Dynamic Radiology of the Abdomen. New York, SpringerVerlag, 1976, p 117; with permission.)

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Figure 30. The sigmoid colon is in continuity with the anterior and posterior pararenal compartments. L = liver; P = pancreas; C = colon. (From Meyers MA: Dynamic Radiology of the Abdomen. New York, Springer-Verlag, 1976, p 186; with permission.)

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Figure 31. Collection of fluid in the right anterior pararenal compartment with viscus displacement. P = pancreas; C = colon; K = kidney. (From Meyers MA: Dynamic Radiology of the Abdomen. New York, Springer-Verlag, 1976, p 131; with permission.)

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artery

Figure 32. Pathway of extravasations from the tail of the pancreas. P = pancreas; C = colon; K = kidney. (From Meyers MA: Dynamic Radiology of the Abdomen. New York, Springer-Verlag, 1976, p 137; with permission.)

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Figure 33. Collection of fluid in the left anterior pararenal space from the pancreas (P), and continuity under and around the cone of renal fascia into the posterior pararenal compartment. K = kidney. (From Meyers MA: Dynamic Radiology of the Abdomen. New York, Springer-Verlag, 1976, p 182; with permission.) Neck and mediastinum

Figure 34. Routes of pancreatic extravasations to the neck, mediastinum, lesser sac, root of the small bowel mesentery, mesentery of the transverse colon, pouch of Douglas, and scrotum through a patent tunica vaginalis. (From Glazer G, Ranson JHC (eds): Acute Pancreatitis. London, Bailliere Tindall, 1988, p 93; with permission.)

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The fusion of the transversalis fascia medially with the muscle fascia demarcates the posterior pararenal space. Thus, it is limited by and parallels the margin of the psoas muscle. No organs are contained within this space. Potential communication with the pre-peritoneal fat of the anterior lateral abdominal wall, however, is possible.

EXTRAVASATIONS OF THE PANCREAS

The pathologic draining of the pancreas, such as in pancreatitis, depends upon the involved part of the organ. However, neither chest nor peritoneal cavity is immune. Occasionally, the scrotum is involved, but primarily the spaces around the kidneys are the first to be occupied by pancreatic fluid. The scope of this article does not permit details, but the reader will understand pancreatic extravasation with the study of Figures 31 to 34.

CONCLUSION

Pancreatic surgery is difficult because of the location of the pancreas and its close relation to the duodenum and the distal common bile duct. This relation produces embryologically, anatomically, and surgically an inseparable unit. We have presented the variations and anomalies of ducts and blood supply in detail. Because of these circumstances, we advise a preoperative selected angiography. References 1. Anacker H: Radiological anatomy of the pancreas. In Anacker H (ed): Efficiency and Limits of Radiologic Examination of the Pancreas, Thieme edition. Acton, MA, Publishing Sciences Group, 1975 2. Baldwin WM: The pancreatic ducts in man, together with a study of the microscopical structure of the minor duodenal papilla. Anat Rec 5:197,1911 , 3. Banting FG, Best CH: The internal secretion of the pancreas. J Lab Clin Med 7:251, 1922 4. Berman LG, Prior JT, Abramov SM, et al: A study of the pancreatic duct system in man by use of vinyl acetate casts of postmortem preparations. Surg Gynecol Obstet 110:391, 1960 5. Beskin CA: Intralobar enteric sequestration of the lung containing aberrant pancreas. J Thorac Cardiovasc Surg 41:314, 1961 6. Bidloo G: Anatomia Humani Corporis. Amstelodami, 1685 7. Bliss WR, et al: Localization of referred pancreatic pain induced by electric stimulation. Gastroenterology 16:317, 1950 8. Boyden EA: The accessory gallbladder. An embryological and comparative study of aberrant biliary vesicles occurring in man and domestic mammals. Am J Anat 38:177, 1926 9. Boyden EA: The sphincter of Oddi in man and certain representative mammals. Surgery 1:25, 1937

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10. Boyden EA: The anatomy of the choledo choduod enal junction in man. Surg Gynecol Obstet 104:641, 1957 11. Boyden EA: In discussio n of Wrenn EL, Favara BE: Duodena l duplicat ion (or pancreat ic bladder) presenti ng as double gallblad der. Surgery 69:858, 1971 12. Burne JC: Pancreat ic and gastric heteroto pia in a diverticu lum of the transver se colon. Journal of Patholog ical Bacteria 75:470,1958 13. Busnard o AC, DiDio LJ, Thomfor d, NR: Anatomi cosurgic al segment s of the human pancreas . Surg Radiol Anat 10:77-82, 1988 14. Carter HS: Portrait of a Surgeon . Glasgow Medical Journal 31:7, 1950 15. Classen M, Koch H, Ruskin H, et al: Pancreat itis after endosco pic retrogra de pancreatography (ERP). Gut 14:431,1973 16. Collins DC: A study of 50,000 specime ns of the human vermifo rm appendix . Surg Gynecol Obstet 101:437, 1955 17. Cotton PB: The normal endosco pic pancreat ogram. Endosco py 6:65, 1974 18. Cubilla AL, Fortner I, Fitzgera ld PJ: Lymph node involvem ent in carcinom a of the head of the pancreas area. Cancer 41:880, 1978 19. Curd H: Histologic study of Meckel's diverticu lum with special reference to heteroto pic tissues. Arch Surg 32:506, 1936 20. de Meyer J: Action de la secretion interne du pancreas sur different s organes et en particuli er sur la secretion renals. Arch di FisioI7:96, 1909 21. Deki H, Sato T: An anatomi c study of the peripanc reatic lymphat ics. Surg Radiol Anat 10:121-135,1988 22. Donatin i B: A systemat ic study of the vascular ization of the pancreas . Surg Radiol Anat 12:173-80,1990 23. Donatin i B, Hidden G: Routes of lymphat ic drainage from the pancreas : A suggeste d segment ation. Surg Radiol Anat 14:35-42, 1992 24. Douglas s TC, Lounsbu ry BF, Cutter WW, et al: An experim ental study of healing in the common bile duct. Surg Gynecol Obstet 91:301, 1950 25. Dowdy GS Jr, Waldron GW, Brown WG: Surgical anatomy of the pancreat obiliary ductal system. Arch Surg 84:229,1962 26. Evans BP, Ochsner A: Gross anatomy of the lymphat ics of the human pancreas . Surgery 36:177,1954 27. Falconer CWA, Griffiths F: Anatom y of the blood vessels in the region of the pancreas . Br J Surg 37:334, 1950 28. Feldman M, Weinber g T: Aberran t pancreas ; cause of duodena l syndrom e. JAMA 148:893,1952 29. Frey CF: Partial and subtotal pancreat ectomy for chronic pancreat itis. In Nyhus LM, Baker RJ (eds): Mastery of Surgery, vol II, ed 2. Boston, Little, Brown, 1992 30. Fry WI, Child CG: Ninety five percent distal pancreat ectomy for chronic pancreat itis. Ann Surg 161:543, 1965 31. Garcia Ferris G, Raul Juan J: Pancreas aberrant e en la pared vesicula r con perforac ion aguda. Prensa Medica Argentin a 58:1829,1971 32. Gross RE: The Surgery of Infancy and Childho od. Philadel phia, WB Saunder s, 1953 33. Gross RE, Chisholm TC: Annular pancreas producin g duodena l obstructi on. Ann Surg 119:759, 1944 34. Harlaftis N, Gray SW, Skandala kis JE: Multiple gallblad ders. Surg Gynecol Obstet 145:928,1977 35. Hayes DM, Greaney EM Jr, Hill JT: Annular pancreas as a cause of acute neonatal duodena l obstructi on. Ann Surg 153:103, 1961 36. Healy JF Jr: A Synopsis of Clinical Anatomy . Philadel phia, WB Saunder s, 1969 37. Horanyi J, Fusy F: Nebenle ber in der Gallenbl asenwan d. Zentralb l Chir 88:768,1963 38. Kasugi T, Kuno N, Kobayas hi S, et al: Endosco pic pancreat ocholang iography . 1. The normal endosco pic pancreat ocholang iogram. Gastroen terology 63:217,1 972 39. Kreel L, Sandin B: Changes in pancreat ic morphol ogy associate d with aging. Gut 14:962,1973 40. Langerh ans P: Beitrage zur mikrosk opischen Anatom ie der Bauchsp eicheldr use. Berlin, G Lange, 1869 41. Lloyd-Jones W, Mountai n JC, Warren KW: Annular pancreas in the adult. Ann Surg 176:163, 1972 42. Melliere D: Variatio ns des arteres hepatiqu es et du carrefou r pancreat ique. J Chir (Paris) 98:5,1968

SURGICAL EMBRYOLOGY AND ANATOMY OF THE PANCREAS

697

43. Meyers MA: Dynamic radiology of the abdomen. In Normal and Pathologic Anatomy. New York, Springer-Verlag, 1976 44. von Mering J, Minkowski 0: Diabetes nach Pankreasextirpation. Archiv fiir Exp Path unl Pharm 26:371,1889 45. Michels NA: The hepatic, cystic, and retroduodenal arteries and their relations to the biliary ducts. Ann Surg 133:503, 1951 46. Michels NA: Blood Supply and Anatomy of the Upper Abdominal Organs. Philadelphia, JB Lippincott, 1955 47. Pearson S: Aberrant pancreas. Review of the literature and report of three cases, one of which produced common and pancreatic duct obstruction. Arch Surg 63:168, 1951 48. Pissas A: Clinical and surgical anatomy studies of the lymphatic circulation of the pancreas. 145:351-366, 1990 49. Ravitch MM: Anomalies of the pancreas. In Carey LC (ed): The Pancreas. St Louis, CV Mosby, 1973 50. Rienhoff WF Jr, Pickerell KL: Pancreatitis: An anatomic study of pancreatic and extrahepatic biliary systems. Arch Surg 51:205,1945 51. Rouvier H: Anatomy of the Human Lymphatic System. Ann Arbor, MI, Edwards Brothers Inc., 1938 52. Santorini JD: Anatomici summi, septemdecim tabulae quas nunc premum edit atque explicat. Parmae ex Regia Typographia, 1775 53. Silen W: Pancreas. In Schwartz SI (ed): Principles of Surgery, vol 2. New York, McGraw-Hill,1964 54. Sivak MV, Sullivan BH: Endoscopic retrograde pancreatography. AnalYSis of the normal pancreatogram. Am J Dig Dis 21:263,1976 55. Skandalakis JE, et al: Identification of vagal structures at the esophageal hiatus. Surgery 75:233,1974 56. Suda K, Mogaki M, Matsumoto Y: Gross dissection and immunohistochemical studies on branch fusion type of ventral and dorsal pancreatic ducts: A case report. Surg Radiol Anat 13:333-337, 1991 57. Thompson 1M: On the arteries and ducts in the hepatic pedicle. A study in statistical human anatomy. Anatomy (University of California) 1:55, 1953 58. Trapnell JE, Howard JM: Transduodenal pancreatography: An improved technique. Surgery 60:1112,1966 59. Triller J, Schweizer W: Angiography and intervention in tumors of the pancreas, liver and bile ducts. RontgenbHitter 42:392-399,1989 60. Varley PF, Rohrmann CA, Silvis SE, et al: The normal endoscopic pancreatogram. Radiology 118:295, 1976 61. Vater A: Dissertatio anatomica, qua novum bilis diverticulum ut et valvulosm colli vesicae felleae constructionem, etc. In Haller's Disputationum Anatomicarum Selectarum, Gottingen III: 2599, 1748 62. Vesalius A: De Humani Corporis Fabrica Libri Septum. Basileae, 1542 63. Warthin AS: Two cases of accessory pancreas (omentum and stomach). The Physician Surgeon (Detroit) 26:337, 1904 64. White TT: Surgical anatomy of the pancreas. In Carey LC (ed): The Pancreas. St. Louis, CV Mosby, 1973 65. Wirsung G: Figura ductus cujusdam cum multiplicibus suis ramulus noviter in Pancreatae Inventis in Diversis Corporibus Humanis. Padua, 1642 66. Wood MD: Anomalous location of the papilla of Vater. Am J Surg 111:265,1966 67. Wrenn EL, Favara BE: Duodenal duplication (or pancreatic bladder) presenting as double gallbladder. Surgery 69:858,1971

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