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Technique of regional subtotal and total pancreatectomy
HOW I DO IT
Technique of Regional Subtotal and Total Pancreatectomy
Joseph G. Fortner, MD, FACS, New York, New York
Cancer surgery is concerned principally with resection of primary tumors with actual or potential regional disease. To accomplish this, the primary site is removed with as much surrounding, apparently noncancerous tissue as is feasible, including en bloc removal of the regional lymphatic drainage basin. Major blood vessels in the region are cleared of lymphatic and soft tissue in the dissection. The anatomic location of the pancreas has prevented application of this basic principle to resections for pancreatic and peripancreatic cancers. As a result, most pancreatic resections for cancer amount to enucleation of a highly malignant neoplasm without regard for regional spread. The portal vein, celiac axis, and hepatic and superior mesenteric arteries are considered “untouchable,” and any involvement of these structures forms the basis for nonresectability. These and other considerations [1-k?] led to the design and development of a pancreatic operation, namely regional pancreatectomy, that conforms to basic principles of cancer surgery. Results of the operation in 61 patients have been reported recently PI. This report describes the technique. An operation in which the pancreatic resection includes an en bloc regional lymph node dissection, peripancreatic soft tissue resection, and resection with reconstruction of the pancreatic segment of portal vein is called a type I regional pancreatectomy. A subtotal or total pancreatectomy may be used. A type II operation is the same operation but with resection and reconstruction of a segment of major artery in the regional dissection (superior mesenteric, hepatic arteries, or the celiac axis). Technique The operation begins with a bilateral subcostal incision that extends from the lateral border of the left rectus muscle to the anterior axillary line on the right. The From Cornell University Medical College and the Gastric and Mixed Tumor Service, Memorial Sloan-Kettering Cancer Center, New York, New York. Requests for reprints should be addressed to Joseph G. Fortner, MO, Department Of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021.
Volume 150, November 1985
abdomen is carefully explored and resectability of the lesion determined. This is carried out by first inspecting and palpating the liver. The peritoneum is examined for seeding. Lymphadenopathy or tumor involvement in the port,a hepatis and celiac axis is sought, the omentum is inspected for metastatic disease, and the periaortic lymph nodes are evaluated with particular attention being paid to the periaortic region at the ligament of Treitz. The latter area is often the only apparent site of metastatic disease. The base of the small bowel mesentery is evaluated for puckering or other involvement. The superior mesenteric vein must be sufficiently uninvolved inferior to the pancreas to permit anastomosis after resection of its pancreatic segment. It should be noted that portal vein involvement in or near the pancreas is not of concern and is not assessed. Any segmental involvement of the superior mesenteric artery, celiac axis, or hepatic artery is evaluated with regard to resection and reconstruction. Anatomic variations, such as the right hepatic artery arising from the superior mesenteric artery and coursing through or near the head of the pancreas, are noted. The tumor is gently palpated at this time without any dissection being performed. The tumor is considered resectable if it is confined to the pancreas on gross examination or if any major vascular involvement is segmental and permits resection and reconstruction. Grossly apparent metastatic disease, such as grossly positive nodes in the porta hepatis or celiac axis, deem the tumor unresectable by this procedure; however, a single grossly positive node immediately adjacent to the pancreas may be an exception. Once resection is decided upon, the abdominal incision is extended to the left anterior axillary line, and wound towels are placed. Regional pancreatectomy type I. Phase I: The omental attachments and the peritoneal reflections of the transverse mesocolon are separated by sharp and blunt dissection down to the colic vascular arcade from the hepatic flexure to just beyond the middle colic vessels. The right colon is then reflected medially and downward by incising t,he hepatocolic ligament. The peritoneum overlying the midportion of the right kidney is incised (Figure l),and the incision is extended inferiorly to the base of the mesocolon and superiorly to the liver where it is carried medially to the inferior vena cava. The peritoneal incision over the kidney is deepened through Gerota’s fascia, and this flap of peritoneum, Gerota’s fascia, and soft tissue are dissected medially with skeletonizing of the
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Figure 7. Wt tissue f/ap Is being developed after reflection of hepatic fiexure. The right kidney and duodenum are being ex-
Figure 3. Tumor can now be safe/y palpated and biopsied.
kidney, renal vessels, ureter, and vena cava (Figure 2). The genital vein is ligated and severed at its origin from the inferior vena cava and distally at the base of the transverse mesocolon. The dissection is continued medially, clearing all soft tissue and lymph nodes in front of and between the vena cava and aorta. The inferior limit of the dissection is the base of the inferior mesenteric artery, which must be carefully preserved in order to maintain the viability of the colon. Continuing to the left, lymphatic and soft tissues are removed from the surface of the aorta. The left renal vein is cleared as it crosses the aorta continuing cephalad until the left half of the vena cava superior to the left renal vein has been skeletonized up to the liver. The right renal artery must be identified and preserved. In some cases, it will be inferior to the left renal vein and can be inadvertently damaged. The base of the superior mesenteric artery and celiac axis are just above the left renal vein but are not seen at this stage of the dissection. Clearing of the base of the celiac axis and superior mesenteric artery will be performed later. For the first time, the extent of the tumor is palpated. This is carried out with the thumb anterior to the tumor mass and the fingers behind the soft tissues that have been reflected (Figure 3). The palpating fingers do not enter into the lymphatic drainage basin of the head of the 594
Figure 2. The soft tissue dissection is progress/~ with exposure of the right renal vein and vena cava. The base of the left renal vein and the aorta are also being exposed, and the duodenum, head of pancreas, and soft tissue are being retracted to the left.
pancreas as is done with the traditional Kocher maneuver. To do so would mitigate the concept of an en bloc dissection. In this instance, the tumor, enclosed in soft tissue, can be palpated readily. A transduodenal needle biopsy may be performed if an intraoperative biopsy is indicated. Phase I of the procedure is then completed, A lap pad is placed after hemostasis has been obtained, and attention is then turned to the porta hepatis. Phase II: This phase begins with a dissection of the gallbladder from its fossa, starting at its fundus and progressing downward but leaving it attached to the common bile duct. The lymphatic vessels and soft tissues to the right of the hepatic duct and portal vein are identified at the liver’s edge, isolated, and transected between ligatures. The dissection continues from the inferior surface of the liver, progressing inferiorly with skeletonization and careful preservation of the common hepatic artery and the hepatic arterial branches. The common hepatic duct is transected immediately below its bifurcation into the right and left hepatic ducts. This is performed after the proximal part of the hepatic duct is occluded with a bulldog clamp and the distal part with a straight Halsted clamp. With transection of the bile duct, circumferential skeletonization of the portal vein is readily accomplished with clearing of all lymphatic vessels and soft tissue from its surface. Lymphatic tissue behind the portal vein must be removed en bloc from the liver downward to its attachment at the superior border of the pancreas. The mass of tissue in the porta hepatis being moved downward from the liver toward the pancreas en bloc includes the gallbladder, distal common hepatic duct, common bile duct, lymphatic vessels, and soft tissues in the porta hepatis. All that remains in the porta hepatis are the skeletonized hepatic arteries, portal vein, and bile ducts (Figure 4). The operation is continued by incising the peritoneum covering the common hepatic artery along its course to the celiac axis. The gastroduodenal artery is identified and dissected free for a sufficient distance so that two ligatures can be placed proximally and one distally before transection. The common hepatic artery is dissected free and cleared of all soft tissue until it joins the celiac axis. In doing this, it is important not to cut into lymph nodes in this area but to find a plane whereby one can incise between normal appearing lymph nodes if at all possible. The American Journal oi Surgery
Regional Subtotal and Total Pancreatectomy
The splenic artery is reached and the left gastric artery is identified nearby. Phase II is now completed. Phase III: Attention is turned to the superior mesenteric vein and transverse mesocolon. Traction is made on the small bowel so as to straighten the base of the small bowel mesentery. The transverse colon is elevated to produce traction on its mesocolon. The course of the superior mesenteric artery in this area is identified by palpation. The vein usually lies anterior and to the right. The anterior surface of the vein is cleared of soft tissue to reveal its bifuration (Figure 5, left). The dissection is then carried cephalad, exposing a large division representing the venous drainage from the upper jejunum. A common trunk is then evident for a variable distance before the pancreas is reached. A sufficient length, usually 3 to 5 cm, of superior mesenteric vein is skeletonized for later occlusion and resection with anastomosis. In the event that the common trunk is too short, either anatomically or from proximity to the tumor, the large proximal jejunal branch can be ligated and divided or anastomosed end-to-side further down on the superior mesenteric vein. During the dissection, the superior mesenteric artery is identified to the left and inferior to the superior mesenteric vein. The peritoneum and lymphatic vessels covering it are incised, and the soft tissue envelopment dissected away to about it,s midportion. A tedious dissection then becomes necessary to transect the lymphatic vessels and soft tissue between the superior mesenteric artery and superior mesenteric vein at their inferior extent. The peritoneal covering, soft tissue, and lymphatic vessels must be cleared circumferentially from both the artery and the vein at these locations. Detachment of the omentum from the transverse colon to the splenic flexure is then completed. Separation of the anterior leaf of the mesocolon from the posterior leaf is continued to the vascular arcade. It is important, not to go further so that the soft tissue covering the surface of the pancreas is left undisturbed. The right, middle, and left colic vessels are ligated and divided, with care being taken to preserve the arcade (Figure 5, right). It should be noted that the vessels in the arcade join at acute angles so that inadvertent occlusion of the vessel’s lumen can occur if the colic vessels are ligated too closely to the arcade. The transverse colon can now be tucked down into the lower portion of the abdominal cavity.
Figure 4. The porta hepatis has been cleared. The transected hepatic duct is occluded by a bulldog clamp. The portal vein has been cleared; an anomalous right hepatic artery goes beneath the portal vein to join the common hepatic artery. The stump of the gastroduodenai artery can also be seen.
The first portion of jejunum is then identified and its mesentery cleared in order to allow transection of the jejunum just distal to the ligament of Treitz. This is performed with the TA 55 stapler using 3.5 mm staples distally and a silk ligature proximally. The proximal cut end of the jejunum is grasped with a Babcock clamp and retracted upward and to the left so that its mesenteric blood supply can be identified, ligated, and divided. The ligament of Treitz and the peritoneal attachments are incised so that the third and fourth portions of the duodenum and a portion of the proximal jejunum can be brought beneath the small bowel mesentery. The posterior parietal peritoneum from the region of the ligament of Treitz is incised upward to near the midportion of the pancreas. The inferior mesenteric vein is doubly ligated and transected. The soft tissues to the right of this incision are then reflected upward and to the right. The previous dissection carried to the left of the aorta is joined so that all the soft tissues in the periaortic region are dissected upward. The periaortic lymphatic vessels at the inferior margin of the dissection should be
Figure 5. Superior mesenteric vein has been cieared( left). Right, middle, and left colic vessels have been ligated and divided preserving the vascular arcade of the transverse colon (right). The base of the transverse mesocolon is attached to the pancreas.
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Figure 6. The line of transection of the stomach is shown atong with the skeletonized structures In the porta hepatis (top teft). The corn mon hepatic artery, celtac axis, left gastric artery, andsplenic artery are evident. Elective lines of transection of the pancreas (top rtght). Transection of the pancreas (bottom teft). The pancreas has been transected (bottom right).
ligated in order to lessen lymphorrhea. The dissection is continued upward to the left renal vein. The stomach is then transected just above its incisura using a TA 90 stapling device with 4.5 mm staples (Figure 6, top left). A vagotomy is usually avoided so as not to disrupt the venous return from the stomach. A decision must be made at this point concerning subtotal versus total pancreatectomy. A minimal margin of at least 4 cm of grossly uninvolved pancreas should be present between the gross limits of the tumor and the line of transection. For most operable cancers of the head of the pancreas, the line of transection can be where the splenic artery joins the pancreas (Figure 6, top right), otherwise the splenic artery should be dissected away from the pancreas for a distance so as to leave at least a 5 cm tail of pancreas or a total pancreatectomy can be performed. For subtotal resections, the pancreas is first rotated to expose the splenic vein posteriorly (Figure 6, bottom left). The vein is isolated in the region to be transected, doubly ligated proximally and once distally, and severed. In most cases, ligation of the splenic vein will have no untoward effects. Since the coronary vein is taken as part of the gorta hepatis and celiac axis dissection, the spleen may become quite large in a few patients and even rupture spontaneously during the operation so that splenectomy becomes necessary. In an occasional patient, the stomach will become hemorrhagic because of venous congestion.
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This occurs only rarely but should not be a cause for alarm. A gastrojejunostomy can be performed with good healing and return of function despite the forbidding appearance of the congested stomach whose venous drainage is the phrenic and periesophageal veins. Fortunately, such congestion is a rare occurrence. Transection of the pancreas is carried out next, with care being taken to avoid injury to the splenic vein or artery. A variety of methods may be used for transecting the pancreas. A stapling device can be used, particularly when the pancreatic duct is small and a ductal anastomosis will not be performed. Another method utilizes the Bovie cautery to transect the pancreas, securing any bleeding vessels and identifying the pancreatic duct for later implantation (Figure 6, bottom right). In the event that a total pancreatectomy is required, the spleen and pancreatic tail and body are dissected free, elevated, and reflected to the right until the celiac axis and portal vein are reached. Short gastric vessels are secured and divided as are the omental attachments to the body and fundus of the stomach. The splenic artery is doubly ligated near the celiac axis, singly ligated distally, and transected. Phase IV The operating surgeon should be standing on the left side of the abdomen. Clearing the superior mesenteric artery of peritoneum, lymphatic vessels, and soft tissue now resumes with unroofing of the soft tissue ante-
The American Journal of Surgery
Regional Subtotal and Total Pancreatectomy
Figure 7. The dissection is continuing to the left of the aorta exposing the base of the ceiiac axis, superior mesenteric artery, and showing the transected left renal vein (top left). The specimen is being retracted to the right. The superior mesenteric artery, ceiiac axis, aorta, and left renal vein have been cleared, and the specimen is retracted to the right (top right). Regions superior to the left renal vein that must be cleared (center ieft). The specimen has been dissected, exposing the superior mesenteric vein, porta/ vein, aorta, and ceiiac axis (center right). The superior mesenteric vein has been occluded with two clamps distally and one clamp near the pancreas (bottom ieft). The portal vein has been occluded before being severed (bottom right).
rior to the artery. The previously begun dissection in phase III is continued downward to the juncture of the superior mesenteric artery with the aorta (Figure 7, top left). The first jejunal branch may or may not be preserved. Soft tissues inferior to the artery are dissected away from the artery being reflected downward and toward the right. Tissues superior to the artery are dissected upward and to the right, until the entire circumference of
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the artery is cleared. It is important to be keenly aware of the one or more branches to the pancreas that will come from the medial aspect of the superior mesenteric artery. The artery is then completely freed of all remaining soft tissue and pancreatic attachments (Figure 7, top right), and dissection of any remnants of lymphatic and soft tissues that may still exist distally between the artery and the superior mesenteric veins is performed.
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Figure 8. Specimen from regIona/ total pancreatectomy.
The periaortic dissection then continues with clearing of the left renal vein and identification of the ganglia lateral to the aorta and surrounding the celiac axis and superior mesenteric artery (Figure 7, center left). These and the lymphatic tissue are cleared from the left side of the aorta and base of the celiac axis and superior mesenteric artery. This dissection is carried medially with clearing of the base of the superior mesenteric artery as well as the space between the celiac axis and superior mesenteric artery. It continues until celiac axis dissection has cleared all lymphatics and soft tissues from the celiac axis and from the aorta in this region (Figure 7, center right). Care must be taken to avoid or secure any phrenic artery which is sometimes encountered in this region. The specimen is retracted to the right and the dissection continues medially and superiorly so that lymphatic vessels and soft tissues in the area which are superior to the left renal vein and between the vena cava and aorta are dissected free, exposing the underlying crura of the diaphragm. The previous phase I dissection is then joined; all soft tissue attachments have been removed and the specimen is attached only by the portal venous system. Vascular occluding clamps are placed distally on the cleared area of superior
mesenteric vein inferior to the pancreas (Figure 7, bottom left) and on the cleared portal vein superior to the pancreas (Figure 7, bottom right). The veins are then transected and the specimen removed (Figure 8). Phase V: The portal venous system is reconstructed as rapidly as possible. This is performed by pushing the base of the small bowel mesentery cephalad until the cut ends of the veins approximate (Figure 9, left and right). One surgical assistant is assigned the task of holding the small bowel mesentery so that there is no tension while the venous anastomosis is being performed. A simple end-toend anastomosis with 5-O silk suture has been used in nearly all cases; however, 5-O Prolene” may be a good alternate. When the anastomosis is completed, the assistant releases the small bowel mesentery. The portal venous system often appears to be too long. Care must be taken while performing this anastomosis that there is no rotation and that the anastomosis is precise (Figure 10). Next, if a subtotal pancreatectomy has been carried out, an end-to-side pancreaticojejunostomy is performed. A variety of methods have been used. The one that appears most satisfactory is a posterior layer of interrupted 4-O silk sutures are placed between the posterior aspect of the cut end of the pancreas and the proximal jejunum near its distal end (Figure 11). The jejunum is opened on its antimesenteric border for the requisite distance. An anterior layer of sutures is placed from the anterior surface of the pancreas to the anterior wall of the jejunum so as to invert the cut end of the pancreas into the lumen of the jejunum. Two or three 4-O silk sutures are placed both anteriorly and posteriorly between the ductal wall and the cut edge of the jejunum. This opens up the pancreatic duct and provides a mucosa-to-mucosa anastomosis. An end-to-side choledochojejunostomy is performed using interrupted 4-O silk sutures of the inverting type. The site of election for this anastomosis is approximately 12 inches from the pancreaticojejunostomy. Then a Billroth II gastrojejunostomy is carried out again approximately 18 inches below the choledochojejunostomy. The small bowel is inspected to be sure there are no kinks and that it is lying correctly in the abdomen. The colon is inspected and laid in its normal position. Any bleeding
Figure 9. The specimen has been removed( left). Occludktg clamps are on the cut end of the portal vein and superior mesenteric vein. The skeletonized superior mesenteric artery is evident /ust beneath them. View is from the left. The base of the small bowel mesentery has been pushed cephalad bringing the ends of the portal vein and superior mesenterlc vein together (rlght).
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The American Journal of Surgery
Regional Subtotal and Total Pancreatectomy
Figure 10. View from the feet kwkk!g cephakd af the superior mesenferlc artery, anasfomosls of the superior mesenterlc vein and portal vein, aorta, vena cava, and base of the small bowel mesentery.
points are identified and secured. Closed drainage using reliavac drains is established. Two drains are placed on the right side, and two on the left side. The abdomen is closed with no. 2 polyglactin (Vicryl”). The skin is approximated with interrupted silver clips. Regional pancreatectomy type II. Arterial considerations: A commonly encountered vascular anomaly, such as an aberrant right hepatic artery, can complicate the operation. The right hepatic artery arises separately from the superior mesenteric artery in about 40 percent of patients [4]. Its course to the liver is often immediately adjacent to the head of the pancreas and through the primary lymphatic drainage basin. Occasionally it will course through the head itself. Dissection of the closely approximated artery is contraindicated because of the danger of spillage of cancer cells. In such instances, the regional dissection is completed as described, but the portion of right hepatic artery adjacent to the pancreas is left attached to the pancreatic lymphatic tissue and pancreas until the portal vein is to be taken. After intraoperative heparinization, the artery is temporarily occluded on either side of the pancreas and transected so as to leave the resected segment attached to the pancreas. It can be reconstructed before or after transection and reconstruction of the portal vein. Reconstruction is carried out with a saphenous vein graft or sometimes by anastomosing the hepatic artery to the gastroduodenal artery or some anomalous branch of the celiac axis. Reconstruction must be performed, otherwise, necrosis of the right hepatic lobe will occur. Involvement of the celiac axis or hepatic artery arising from the celiac axis must be localized to one area for surgical resection to be considered. This type of localized extension is often at or near the takeoff of the gastroduodenal artery. The involved area can be isolated and transected between vascular occluding clamps so that the involved portion is left attached to the pancreas and the en bloc status is undisturbed. Reconstruction can often be carried out by approximating the two ends and shortening the vessels total length or a vein graft can be used. Localized direct extension of some pancreatic cancers will involve a segment of superior mesenteric artery. In
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Figure 11. Pancreatlcojejunostomy. a: Posterior row of sutures are in place. Sutures are being placed in wall of pancreatic duct and bowel. Anterior row of sutures have been placed lo approxC mate anterlor aspect of pancreas with jejunum. b: Close-up of pancreatic duct anastomosla Posterior sutures fled. Anterior sutures In place. c: Completed anastomosis.
dealing with this, the artery is cleared of lymphatic and soft tissues proximally and distally to the area of involvement. A jejunal branch of the artery is isolated and a small catheter inserted to perfuse the intestine. Chilled Ringer’s lactate solution containing 1,000 units of heparin per liter is infused slowly. The superior mesenteric artery is temporarily occluded proximally with vascular clamps and the artery transected proximal to the tumor. It is then transected distal to the tumor to leave the involved artery attached to the specimen. The portal vein is next occluded above the pancreas and transected, the superior mesenteric vein is transected below the pancreas without occlusion, and the en bloc dissected specimen is removed. Administration of Ringer’s lactate solution is speeded up and the bowel vasculature flushed with the effluent coming out of the transected superior mesenteric vein. One then has, in effect, an autotransplant of intestine. The artery can then be reconstructed leisurely using 5-O Prolenee for an end-to-end anastomosis of the distal superior mesenteric artery to the preserved base of superior mesenteric artery or to the distal aorta. The superior mesenteric vein is anastomosed to the portal vein with the perfusion being stopped just before completion of the venous anastomosis. After completion of the venous anastomosis, all occluding clamps are removed and the blood supply to the intestine is reconstituted. Systemic heparinization is not carried out. Postoperative management: The regionally pancreatectomized patient is managed as any other person who has undergone a major surgical procedure but with some special considerations. During the first 2 or 3 days, there
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may be a 2,000 or 3,000 ml loss from the abdominal drains. This is a lymphorrhea and should be replaced milliliter for milliliter with fresh frozen plasma containing clotting factors. It is particularly important to know that this profuse drainage usually diminishes suddenly, and continued administration of large amounts of plasma can lead to fluid overload. Management of the patient’s diabetic state after regional total pancreatectomy involves insulin coverage of administered glucose, with insulin administration being dependent on blood glucose levels and fractional urinalysis. Resumption of oral nutritional intake usually on the 5th to 10th postoperative day should include pancreatic enzyme replacement with pancrelipase (Pancrease@ or Cotazym@), and if frequent bowel movements are present, diphenoxylate (Lomotil@‘) may be added. Anorexia can occur with variable severity and patients must be taught to eat at prescribed times. Nutritional supplements such as Sustacal@ are valuable aids to achieve sufficient caloric intake. Some patients will require intravenous alimentation for 1 to 2 or more weeks before they are able to take in sufficient calories by mouth. Appetite returns and bowel habits become or approach normal after a few months.
Summary The technique of regional pancreatectomy as detailed is divided into five phases. The procedure
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includes en bloc regional lymph node dissection, peripancreatic soft tissue resection, and resection with reconstruction of the pancreatic segment of portal vein. The pancreatic resection can be subtotal or total.
References 1. Fortner JG. Regional resection of cancer of the pancreas. A new surgical approach. Surgery 1973;73:307-20. 2. Former JG. Recent advances in pancreatic cancer. Surg Clin North Am 1974;54:859-63. 3. Former JG. Cancer of the pancreas (letter to the editor). New Engl J Med 1980;302:232. 4. Fortner JG. Median arcuate ligament obstruction of celiac axis and pancreatic cancer. Ann Surg 1981;194:698-700. 5. Fortner JG. Surgical principles for pancreatic cancer: regional total and subtotal pancreatectomy. Cancer 1981;47:1712-8. 6. Fortner JG. Regional pancreatectomy for cancer of the pancreas, ampulla and other related sites: tumor staging and results. Ann Surg 1984;199:418-25. 7. Former JG, Kim DK. Regional pancreatectomy (16 mm movie, color), Philadelphia: Smith, Kline, and French (sponsor) 1976. 8. Fortner JG, Kim DK, Cubilla A, Turnbull A, Pahnke LD, Shils ME. Regional pancreatectomy: en bloc pancreatic, portal vein and lymph node resection. Ann Surg 1977;186:42-50.
The Amerlcan Journal of Surgery
Technique of Regional Subtotal and Total Pancreatectomy
Joseph G. Fortner, MD, FACS, New York, New York
Cancer surgery is concerned principally with resection of primary tumors with actual or potential regional disease. To accomplish this, the primary site is removed with as much surrounding, apparently noncancerous tissue as is feasible, including en bloc removal of the regional lymphatic drainage basin. Major blood vessels in the region are cleared of lymphatic and soft tissue in the dissection. The anatomic location of the pancreas has prevented application of this basic principle to resections for pancreatic and peripancreatic cancers. As a result, most pancreatic resections for cancer amount to enucleation of a highly malignant neoplasm without regard for regional spread. The portal vein, celiac axis, and hepatic and superior mesenteric arteries are considered “untouchable,” and any involvement of these structures forms the basis for nonresectability. These and other considerations [1-k?] led to the design and development of a pancreatic operation, namely regional pancreatectomy, that conforms to basic principles of cancer surgery. Results of the operation in 61 patients have been reported recently PI. This report describes the technique. An operation in which the pancreatic resection includes an en bloc regional lymph node dissection, peripancreatic soft tissue resection, and resection with reconstruction of the pancreatic segment of portal vein is called a type I regional pancreatectomy. A subtotal or total pancreatectomy may be used. A type II operation is the same operation but with resection and reconstruction of a segment of major artery in the regional dissection (superior mesenteric, hepatic arteries, or the celiac axis). Technique The operation begins with a bilateral subcostal incision that extends from the lateral border of the left rectus muscle to the anterior axillary line on the right. The From Cornell University Medical College and the Gastric and Mixed Tumor Service, Memorial Sloan-Kettering Cancer Center, New York, New York. Requests for reprints should be addressed to Joseph G. Fortner, MO, Department Of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021.
Volume 150, November 1985
abdomen is carefully explored and resectability of the lesion determined. This is carried out by first inspecting and palpating the liver. The peritoneum is examined for seeding. Lymphadenopathy or tumor involvement in the port,a hepatis and celiac axis is sought, the omentum is inspected for metastatic disease, and the periaortic lymph nodes are evaluated with particular attention being paid to the periaortic region at the ligament of Treitz. The latter area is often the only apparent site of metastatic disease. The base of the small bowel mesentery is evaluated for puckering or other involvement. The superior mesenteric vein must be sufficiently uninvolved inferior to the pancreas to permit anastomosis after resection of its pancreatic segment. It should be noted that portal vein involvement in or near the pancreas is not of concern and is not assessed. Any segmental involvement of the superior mesenteric artery, celiac axis, or hepatic artery is evaluated with regard to resection and reconstruction. Anatomic variations, such as the right hepatic artery arising from the superior mesenteric artery and coursing through or near the head of the pancreas, are noted. The tumor is gently palpated at this time without any dissection being performed. The tumor is considered resectable if it is confined to the pancreas on gross examination or if any major vascular involvement is segmental and permits resection and reconstruction. Grossly apparent metastatic disease, such as grossly positive nodes in the porta hepatis or celiac axis, deem the tumor unresectable by this procedure; however, a single grossly positive node immediately adjacent to the pancreas may be an exception. Once resection is decided upon, the abdominal incision is extended to the left anterior axillary line, and wound towels are placed. Regional pancreatectomy type I. Phase I: The omental attachments and the peritoneal reflections of the transverse mesocolon are separated by sharp and blunt dissection down to the colic vascular arcade from the hepatic flexure to just beyond the middle colic vessels. The right colon is then reflected medially and downward by incising t,he hepatocolic ligament. The peritoneum overlying the midportion of the right kidney is incised (Figure l),and the incision is extended inferiorly to the base of the mesocolon and superiorly to the liver where it is carried medially to the inferior vena cava. The peritoneal incision over the kidney is deepened through Gerota’s fascia, and this flap of peritoneum, Gerota’s fascia, and soft tissue are dissected medially with skeletonizing of the
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Figure 7. Wt tissue f/ap Is being developed after reflection of hepatic fiexure. The right kidney and duodenum are being ex-
Figure 3. Tumor can now be safe/y palpated and biopsied.
kidney, renal vessels, ureter, and vena cava (Figure 2). The genital vein is ligated and severed at its origin from the inferior vena cava and distally at the base of the transverse mesocolon. The dissection is continued medially, clearing all soft tissue and lymph nodes in front of and between the vena cava and aorta. The inferior limit of the dissection is the base of the inferior mesenteric artery, which must be carefully preserved in order to maintain the viability of the colon. Continuing to the left, lymphatic and soft tissues are removed from the surface of the aorta. The left renal vein is cleared as it crosses the aorta continuing cephalad until the left half of the vena cava superior to the left renal vein has been skeletonized up to the liver. The right renal artery must be identified and preserved. In some cases, it will be inferior to the left renal vein and can be inadvertently damaged. The base of the superior mesenteric artery and celiac axis are just above the left renal vein but are not seen at this stage of the dissection. Clearing of the base of the celiac axis and superior mesenteric artery will be performed later. For the first time, the extent of the tumor is palpated. This is carried out with the thumb anterior to the tumor mass and the fingers behind the soft tissues that have been reflected (Figure 3). The palpating fingers do not enter into the lymphatic drainage basin of the head of the 594
Figure 2. The soft tissue dissection is progress/~ with exposure of the right renal vein and vena cava. The base of the left renal vein and the aorta are also being exposed, and the duodenum, head of pancreas, and soft tissue are being retracted to the left.
pancreas as is done with the traditional Kocher maneuver. To do so would mitigate the concept of an en bloc dissection. In this instance, the tumor, enclosed in soft tissue, can be palpated readily. A transduodenal needle biopsy may be performed if an intraoperative biopsy is indicated. Phase I of the procedure is then completed, A lap pad is placed after hemostasis has been obtained, and attention is then turned to the porta hepatis. Phase II: This phase begins with a dissection of the gallbladder from its fossa, starting at its fundus and progressing downward but leaving it attached to the common bile duct. The lymphatic vessels and soft tissues to the right of the hepatic duct and portal vein are identified at the liver’s edge, isolated, and transected between ligatures. The dissection continues from the inferior surface of the liver, progressing inferiorly with skeletonization and careful preservation of the common hepatic artery and the hepatic arterial branches. The common hepatic duct is transected immediately below its bifurcation into the right and left hepatic ducts. This is performed after the proximal part of the hepatic duct is occluded with a bulldog clamp and the distal part with a straight Halsted clamp. With transection of the bile duct, circumferential skeletonization of the portal vein is readily accomplished with clearing of all lymphatic vessels and soft tissue from its surface. Lymphatic tissue behind the portal vein must be removed en bloc from the liver downward to its attachment at the superior border of the pancreas. The mass of tissue in the porta hepatis being moved downward from the liver toward the pancreas en bloc includes the gallbladder, distal common hepatic duct, common bile duct, lymphatic vessels, and soft tissues in the porta hepatis. All that remains in the porta hepatis are the skeletonized hepatic arteries, portal vein, and bile ducts (Figure 4). The operation is continued by incising the peritoneum covering the common hepatic artery along its course to the celiac axis. The gastroduodenal artery is identified and dissected free for a sufficient distance so that two ligatures can be placed proximally and one distally before transection. The common hepatic artery is dissected free and cleared of all soft tissue until it joins the celiac axis. In doing this, it is important not to cut into lymph nodes in this area but to find a plane whereby one can incise between normal appearing lymph nodes if at all possible. The American Journal oi Surgery
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The splenic artery is reached and the left gastric artery is identified nearby. Phase II is now completed. Phase III: Attention is turned to the superior mesenteric vein and transverse mesocolon. Traction is made on the small bowel so as to straighten the base of the small bowel mesentery. The transverse colon is elevated to produce traction on its mesocolon. The course of the superior mesenteric artery in this area is identified by palpation. The vein usually lies anterior and to the right. The anterior surface of the vein is cleared of soft tissue to reveal its bifuration (Figure 5, left). The dissection is then carried cephalad, exposing a large division representing the venous drainage from the upper jejunum. A common trunk is then evident for a variable distance before the pancreas is reached. A sufficient length, usually 3 to 5 cm, of superior mesenteric vein is skeletonized for later occlusion and resection with anastomosis. In the event that the common trunk is too short, either anatomically or from proximity to the tumor, the large proximal jejunal branch can be ligated and divided or anastomosed end-to-side further down on the superior mesenteric vein. During the dissection, the superior mesenteric artery is identified to the left and inferior to the superior mesenteric vein. The peritoneum and lymphatic vessels covering it are incised, and the soft tissue envelopment dissected away to about it,s midportion. A tedious dissection then becomes necessary to transect the lymphatic vessels and soft tissue between the superior mesenteric artery and superior mesenteric vein at their inferior extent. The peritoneal covering, soft tissue, and lymphatic vessels must be cleared circumferentially from both the artery and the vein at these locations. Detachment of the omentum from the transverse colon to the splenic flexure is then completed. Separation of the anterior leaf of the mesocolon from the posterior leaf is continued to the vascular arcade. It is important, not to go further so that the soft tissue covering the surface of the pancreas is left undisturbed. The right, middle, and left colic vessels are ligated and divided, with care being taken to preserve the arcade (Figure 5, right). It should be noted that the vessels in the arcade join at acute angles so that inadvertent occlusion of the vessel’s lumen can occur if the colic vessels are ligated too closely to the arcade. The transverse colon can now be tucked down into the lower portion of the abdominal cavity.
Figure 4. The porta hepatis has been cleared. The transected hepatic duct is occluded by a bulldog clamp. The portal vein has been cleared; an anomalous right hepatic artery goes beneath the portal vein to join the common hepatic artery. The stump of the gastroduodenai artery can also be seen.
The first portion of jejunum is then identified and its mesentery cleared in order to allow transection of the jejunum just distal to the ligament of Treitz. This is performed with the TA 55 stapler using 3.5 mm staples distally and a silk ligature proximally. The proximal cut end of the jejunum is grasped with a Babcock clamp and retracted upward and to the left so that its mesenteric blood supply can be identified, ligated, and divided. The ligament of Treitz and the peritoneal attachments are incised so that the third and fourth portions of the duodenum and a portion of the proximal jejunum can be brought beneath the small bowel mesentery. The posterior parietal peritoneum from the region of the ligament of Treitz is incised upward to near the midportion of the pancreas. The inferior mesenteric vein is doubly ligated and transected. The soft tissues to the right of this incision are then reflected upward and to the right. The previous dissection carried to the left of the aorta is joined so that all the soft tissues in the periaortic region are dissected upward. The periaortic lymphatic vessels at the inferior margin of the dissection should be
Figure 5. Superior mesenteric vein has been cieared( left). Right, middle, and left colic vessels have been ligated and divided preserving the vascular arcade of the transverse colon (right). The base of the transverse mesocolon is attached to the pancreas.
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Figure 6. The line of transection of the stomach is shown atong with the skeletonized structures In the porta hepatis (top teft). The corn mon hepatic artery, celtac axis, left gastric artery, andsplenic artery are evident. Elective lines of transection of the pancreas (top rtght). Transection of the pancreas (bottom teft). The pancreas has been transected (bottom right).
ligated in order to lessen lymphorrhea. The dissection is continued upward to the left renal vein. The stomach is then transected just above its incisura using a TA 90 stapling device with 4.5 mm staples (Figure 6, top left). A vagotomy is usually avoided so as not to disrupt the venous return from the stomach. A decision must be made at this point concerning subtotal versus total pancreatectomy. A minimal margin of at least 4 cm of grossly uninvolved pancreas should be present between the gross limits of the tumor and the line of transection. For most operable cancers of the head of the pancreas, the line of transection can be where the splenic artery joins the pancreas (Figure 6, top right), otherwise the splenic artery should be dissected away from the pancreas for a distance so as to leave at least a 5 cm tail of pancreas or a total pancreatectomy can be performed. For subtotal resections, the pancreas is first rotated to expose the splenic vein posteriorly (Figure 6, bottom left). The vein is isolated in the region to be transected, doubly ligated proximally and once distally, and severed. In most cases, ligation of the splenic vein will have no untoward effects. Since the coronary vein is taken as part of the gorta hepatis and celiac axis dissection, the spleen may become quite large in a few patients and even rupture spontaneously during the operation so that splenectomy becomes necessary. In an occasional patient, the stomach will become hemorrhagic because of venous congestion.
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This occurs only rarely but should not be a cause for alarm. A gastrojejunostomy can be performed with good healing and return of function despite the forbidding appearance of the congested stomach whose venous drainage is the phrenic and periesophageal veins. Fortunately, such congestion is a rare occurrence. Transection of the pancreas is carried out next, with care being taken to avoid injury to the splenic vein or artery. A variety of methods may be used for transecting the pancreas. A stapling device can be used, particularly when the pancreatic duct is small and a ductal anastomosis will not be performed. Another method utilizes the Bovie cautery to transect the pancreas, securing any bleeding vessels and identifying the pancreatic duct for later implantation (Figure 6, bottom right). In the event that a total pancreatectomy is required, the spleen and pancreatic tail and body are dissected free, elevated, and reflected to the right until the celiac axis and portal vein are reached. Short gastric vessels are secured and divided as are the omental attachments to the body and fundus of the stomach. The splenic artery is doubly ligated near the celiac axis, singly ligated distally, and transected. Phase IV The operating surgeon should be standing on the left side of the abdomen. Clearing the superior mesenteric artery of peritoneum, lymphatic vessels, and soft tissue now resumes with unroofing of the soft tissue ante-
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Figure 7. The dissection is continuing to the left of the aorta exposing the base of the ceiiac axis, superior mesenteric artery, and showing the transected left renal vein (top left). The specimen is being retracted to the right. The superior mesenteric artery, ceiiac axis, aorta, and left renal vein have been cleared, and the specimen is retracted to the right (top right). Regions superior to the left renal vein that must be cleared (center ieft). The specimen has been dissected, exposing the superior mesenteric vein, porta/ vein, aorta, and ceiiac axis (center right). The superior mesenteric vein has been occluded with two clamps distally and one clamp near the pancreas (bottom ieft). The portal vein has been occluded before being severed (bottom right).
rior to the artery. The previously begun dissection in phase III is continued downward to the juncture of the superior mesenteric artery with the aorta (Figure 7, top left). The first jejunal branch may or may not be preserved. Soft tissues inferior to the artery are dissected away from the artery being reflected downward and toward the right. Tissues superior to the artery are dissected upward and to the right, until the entire circumference of
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the artery is cleared. It is important to be keenly aware of the one or more branches to the pancreas that will come from the medial aspect of the superior mesenteric artery. The artery is then completely freed of all remaining soft tissue and pancreatic attachments (Figure 7, top right), and dissection of any remnants of lymphatic and soft tissues that may still exist distally between the artery and the superior mesenteric veins is performed.
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Figure 8. Specimen from regIona/ total pancreatectomy.
The periaortic dissection then continues with clearing of the left renal vein and identification of the ganglia lateral to the aorta and surrounding the celiac axis and superior mesenteric artery (Figure 7, center left). These and the lymphatic tissue are cleared from the left side of the aorta and base of the celiac axis and superior mesenteric artery. This dissection is carried medially with clearing of the base of the superior mesenteric artery as well as the space between the celiac axis and superior mesenteric artery. It continues until celiac axis dissection has cleared all lymphatics and soft tissues from the celiac axis and from the aorta in this region (Figure 7, center right). Care must be taken to avoid or secure any phrenic artery which is sometimes encountered in this region. The specimen is retracted to the right and the dissection continues medially and superiorly so that lymphatic vessels and soft tissues in the area which are superior to the left renal vein and between the vena cava and aorta are dissected free, exposing the underlying crura of the diaphragm. The previous phase I dissection is then joined; all soft tissue attachments have been removed and the specimen is attached only by the portal venous system. Vascular occluding clamps are placed distally on the cleared area of superior
mesenteric vein inferior to the pancreas (Figure 7, bottom left) and on the cleared portal vein superior to the pancreas (Figure 7, bottom right). The veins are then transected and the specimen removed (Figure 8). Phase V: The portal venous system is reconstructed as rapidly as possible. This is performed by pushing the base of the small bowel mesentery cephalad until the cut ends of the veins approximate (Figure 9, left and right). One surgical assistant is assigned the task of holding the small bowel mesentery so that there is no tension while the venous anastomosis is being performed. A simple end-toend anastomosis with 5-O silk suture has been used in nearly all cases; however, 5-O Prolene” may be a good alternate. When the anastomosis is completed, the assistant releases the small bowel mesentery. The portal venous system often appears to be too long. Care must be taken while performing this anastomosis that there is no rotation and that the anastomosis is precise (Figure 10). Next, if a subtotal pancreatectomy has been carried out, an end-to-side pancreaticojejunostomy is performed. A variety of methods have been used. The one that appears most satisfactory is a posterior layer of interrupted 4-O silk sutures are placed between the posterior aspect of the cut end of the pancreas and the proximal jejunum near its distal end (Figure 11). The jejunum is opened on its antimesenteric border for the requisite distance. An anterior layer of sutures is placed from the anterior surface of the pancreas to the anterior wall of the jejunum so as to invert the cut end of the pancreas into the lumen of the jejunum. Two or three 4-O silk sutures are placed both anteriorly and posteriorly between the ductal wall and the cut edge of the jejunum. This opens up the pancreatic duct and provides a mucosa-to-mucosa anastomosis. An end-to-side choledochojejunostomy is performed using interrupted 4-O silk sutures of the inverting type. The site of election for this anastomosis is approximately 12 inches from the pancreaticojejunostomy. Then a Billroth II gastrojejunostomy is carried out again approximately 18 inches below the choledochojejunostomy. The small bowel is inspected to be sure there are no kinks and that it is lying correctly in the abdomen. The colon is inspected and laid in its normal position. Any bleeding
Figure 9. The specimen has been removed( left). Occludktg clamps are on the cut end of the portal vein and superior mesenteric vein. The skeletonized superior mesenteric artery is evident /ust beneath them. View is from the left. The base of the small bowel mesentery has been pushed cephalad bringing the ends of the portal vein and superior mesenterlc vein together (rlght).
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Figure 10. View from the feet kwkk!g cephakd af the superior mesenferlc artery, anasfomosls of the superior mesenterlc vein and portal vein, aorta, vena cava, and base of the small bowel mesentery.
points are identified and secured. Closed drainage using reliavac drains is established. Two drains are placed on the right side, and two on the left side. The abdomen is closed with no. 2 polyglactin (Vicryl”). The skin is approximated with interrupted silver clips. Regional pancreatectomy type II. Arterial considerations: A commonly encountered vascular anomaly, such as an aberrant right hepatic artery, can complicate the operation. The right hepatic artery arises separately from the superior mesenteric artery in about 40 percent of patients [4]. Its course to the liver is often immediately adjacent to the head of the pancreas and through the primary lymphatic drainage basin. Occasionally it will course through the head itself. Dissection of the closely approximated artery is contraindicated because of the danger of spillage of cancer cells. In such instances, the regional dissection is completed as described, but the portion of right hepatic artery adjacent to the pancreas is left attached to the pancreatic lymphatic tissue and pancreas until the portal vein is to be taken. After intraoperative heparinization, the artery is temporarily occluded on either side of the pancreas and transected so as to leave the resected segment attached to the pancreas. It can be reconstructed before or after transection and reconstruction of the portal vein. Reconstruction is carried out with a saphenous vein graft or sometimes by anastomosing the hepatic artery to the gastroduodenal artery or some anomalous branch of the celiac axis. Reconstruction must be performed, otherwise, necrosis of the right hepatic lobe will occur. Involvement of the celiac axis or hepatic artery arising from the celiac axis must be localized to one area for surgical resection to be considered. This type of localized extension is often at or near the takeoff of the gastroduodenal artery. The involved area can be isolated and transected between vascular occluding clamps so that the involved portion is left attached to the pancreas and the en bloc status is undisturbed. Reconstruction can often be carried out by approximating the two ends and shortening the vessels total length or a vein graft can be used. Localized direct extension of some pancreatic cancers will involve a segment of superior mesenteric artery. In
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Figure 11. Pancreatlcojejunostomy. a: Posterior row of sutures are in place. Sutures are being placed in wall of pancreatic duct and bowel. Anterior row of sutures have been placed lo approxC mate anterlor aspect of pancreas with jejunum. b: Close-up of pancreatic duct anastomosla Posterior sutures fled. Anterior sutures In place. c: Completed anastomosis.
dealing with this, the artery is cleared of lymphatic and soft tissues proximally and distally to the area of involvement. A jejunal branch of the artery is isolated and a small catheter inserted to perfuse the intestine. Chilled Ringer’s lactate solution containing 1,000 units of heparin per liter is infused slowly. The superior mesenteric artery is temporarily occluded proximally with vascular clamps and the artery transected proximal to the tumor. It is then transected distal to the tumor to leave the involved artery attached to the specimen. The portal vein is next occluded above the pancreas and transected, the superior mesenteric vein is transected below the pancreas without occlusion, and the en bloc dissected specimen is removed. Administration of Ringer’s lactate solution is speeded up and the bowel vasculature flushed with the effluent coming out of the transected superior mesenteric vein. One then has, in effect, an autotransplant of intestine. The artery can then be reconstructed leisurely using 5-O Prolenee for an end-to-end anastomosis of the distal superior mesenteric artery to the preserved base of superior mesenteric artery or to the distal aorta. The superior mesenteric vein is anastomosed to the portal vein with the perfusion being stopped just before completion of the venous anastomosis. After completion of the venous anastomosis, all occluding clamps are removed and the blood supply to the intestine is reconstituted. Systemic heparinization is not carried out. Postoperative management: The regionally pancreatectomized patient is managed as any other person who has undergone a major surgical procedure but with some special considerations. During the first 2 or 3 days, there
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may be a 2,000 or 3,000 ml loss from the abdominal drains. This is a lymphorrhea and should be replaced milliliter for milliliter with fresh frozen plasma containing clotting factors. It is particularly important to know that this profuse drainage usually diminishes suddenly, and continued administration of large amounts of plasma can lead to fluid overload. Management of the patient’s diabetic state after regional total pancreatectomy involves insulin coverage of administered glucose, with insulin administration being dependent on blood glucose levels and fractional urinalysis. Resumption of oral nutritional intake usually on the 5th to 10th postoperative day should include pancreatic enzyme replacement with pancrelipase (Pancrease@ or Cotazym@), and if frequent bowel movements are present, diphenoxylate (Lomotil@‘) may be added. Anorexia can occur with variable severity and patients must be taught to eat at prescribed times. Nutritional supplements such as Sustacal@ are valuable aids to achieve sufficient caloric intake. Some patients will require intravenous alimentation for 1 to 2 or more weeks before they are able to take in sufficient calories by mouth. Appetite returns and bowel habits become or approach normal after a few months.
Summary The technique of regional pancreatectomy as detailed is divided into five phases. The procedure
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includes en bloc regional lymph node dissection, peripancreatic soft tissue resection, and resection with reconstruction of the pancreatic segment of portal vein. The pancreatic resection can be subtotal or total.
References 1. Fortner JG. Regional resection of cancer of the pancreas. A new surgical approach. Surgery 1973;73:307-20. 2. Former JG. Recent advances in pancreatic cancer. Surg Clin North Am 1974;54:859-63. 3. Former JG. Cancer of the pancreas (letter to the editor). New Engl J Med 1980;302:232. 4. Fortner JG. Median arcuate ligament obstruction of celiac axis and pancreatic cancer. Ann Surg 1981;194:698-700. 5. Fortner JG. Surgical principles for pancreatic cancer: regional total and subtotal pancreatectomy. Cancer 1981;47:1712-8. 6. Fortner JG. Regional pancreatectomy for cancer of the pancreas, ampulla and other related sites: tumor staging and results. Ann Surg 1984;199:418-25. 7. Former JG, Kim DK. Regional pancreatectomy (16 mm movie, color), Philadelphia: Smith, Kline, and French (sponsor) 1976. 8. Fortner JG, Kim DK, Cubilla A, Turnbull A, Pahnke LD, Shils ME. Regional pancreatectomy: en bloc pancreatic, portal vein and lymph node resection. Ann Surg 1977;186:42-50.
The Amerlcan Journal of Surgery