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Computed tomography after radical pancreaticoduodenectomy (Whipple's procedure)
Clinical Radiology (2008) 63, 921e928
PICTORIAL REVIEW
Computed tomography after radical pancreaticoduodenectomy (Whipple’s procedure) S.L. Smitha,*, F. Hampsonb, M. Duxburyc, D.M. Raed, M.T. Sinclaird Departments of aRadiology, and dPancreaticobiliary surgery, Ipswich Hospital, Ipswich, IP4 5PD, UK, b Department of Radiology, Addenbrooke’s Hospital NHS Trust, Cambridge, UK, cDepartment of Surgery, Royal Infirmary of Edinburgh, Little France, Edinburgh EH16 4SU, UK Received 31 July 2007; received in revised form 24 September 2007; accepted 8 October 2007
Whipple’s procedure (radical pancreaticoduodenectomy) is currently the only curative option for patients with periampullary malignancy. The surgery is highly complex and involves multiple anastomoses. Complications are common and can lead to significant postoperative morbidity. Early detection and treatment of complications is vital, and highquality multidetector computed tomography (MDCT) is currently the best method of investigation. This review outlines the surgical technique and illustrates the range of normal postoperative appearances together with the common complications. ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Pancreatic cancer is the fourth leading cause of death due to malignant disease in adults.1 The disease is usually either locally advanced or metastatic at presentation, and less than 20% of patients have disease confined to the pancreas. In this group radical surgery offers the only realistic chance of cure. Classical pancreaticoduodenectomy (Whipple’s procedure) involves complex and aggressive surgery. In the best hands the procedure caries a 1e5% mortality and outcomes have improved in centres that undertake large numbers of resections. Despite the improved mortality statistics there remains a significant postoperative morbidity, estimated to be between 20e30%. In one large series of 650 pancreaticoduodenectomies, a postoperative complication rate of 41e47% was reported.2 Even in those with technically successful surgery the 5-year * Guarantor and correspondent: S.L. Smith, Department of Radiology, Ipswich Hospital, Ipswich, IP4 5PD, UK. Tel.: þ44 1473 703380; fax: þ44 1473 270655. E-mail address: [email protected] (S.L. Smith).
survival for those patients with pancreatic head carcinoma is less than 5%, with the majority of deaths occurring because of recurrent disease. The outcome for other periampullary tumours, namely distal duct cholangiocarcinoma and ampullary carcinoma, is better, reflecting the less locally aggressive nature of these malignancies. Both the early detection of postoperative complications and identification of later disease recurrence are vital. Radiology and, in particular, high-quality multidetector computed tomography (MDCT) studies have a pivotal role here. The aim of the present review is to illustrate normal postoperative CT appearances, as well as complications seen after surgery.
Whipple’s procedure Pancreaticoduodenectomy is indicated primarily for two conditions: tumour in the periampullary region (cancer in the head of pancreas, the ampulla of Vater, the distal bile duct, and the duodenum) and chronic pancreatitis involving the head and uncinate process of the pancreas.
0009-9260/$ - see front matter ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2007.10.012
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Using a rooftop or bilateral subcostal incision, an extensive Kocher manoeuvre is performed to mobilize the duodenum and head of pancreas from the inferior vena cava and aorta. The transverse mesocolon is mobilized from the head and uncinate process of the pancreas to expose the superior mesenteric vein, which is traced to the neck of the pancreas. The dissection is continued to expose the plane between the pancreas and the superior mesenteric and portal veins. The extensive mobilization of the head of pancreas is important to determine the extent of tumour spread to adjacent structures, and hence its resectability. The gallbladder is excised and the common duct is divided to expose the portal vein. The lesser curve of the stomach is prepared for transection. A window is created above the incisura after dividing the branches of the left gastric artery. The greater omentum is divided and an area on the greater curvature of the stomach is prepared by division of the gastroepiploic vessels. The stomach is transected with a linear stapler. The antrum of the stomach is rotated to the right to expose the head and neck of the pancreas. The gastroduodenal artery is exposed and divided. The pancreatic neck is then divided. The ligament of Treitz is mobilized and the jejunum is divided with a linear stapler. The proximal jejunum is passed behind the superior mesenteric vessels to the patient’s right. This helps the dissection of the uncinate process from the superior mesenteric vein. Multiple vessels between the uncinate process and the superior mesenteric vessels are ligated. The resected specimen consists of the gallbladder, the distal common bile duct, duodenum, and proximal jejunum, and the head, neck and uncinate process of the pancreas. Surgical reconstruction consists of a pancreaticoenterostomy, a choledochojejunostomy, and a gastrojejunostomy. A pancreaticoenterostomy can be performed by mucosa-to-mucosa anastomosis with the jejunum or the posterior wall of the stomach. A pancreatic duct stent is usually inserted across the anastomosis using an 8 F infant feeding tube. The choledochojejunostomy is performed by an end-to-side anastomosis. Finally, a retrocolic gastrojejunostomy is performed on the posterior wall of the stomach near its greater curvature (Fig. 1). A drain is placed near the pancreaticoenterostomy and a feeding jejunostomy is performed.
Postoperative CT technique CT is usually performed in the immediate postoperative period because of persistent pyrexia, raised inflammatory markers, or abnormal serum
S.L. Smith et al.
Figure 1 Schematic of standard Whipple’s operation. Anastomoses/suture lines: (A) choledochojejunostomy, (B) pancreaticojejunostomy, (C) gastrojejunostomy, (D) sutured proximal limb of jejunostomy.
bilirubin. Imaging parameters should be adjusted to ensure fine detector collimation (ideally 1 mm section thickness) to facilitate multiplanar reconstructions. At our institution a pragmatic approach to oral contrast medium is used. If relatively healthy, patients receive 700 ml 2% Gastrograffin (Schering Health Care Ltd, Burgess Hill, West Sussex, UK) 30 min before the procedure. It is important to attempt to fill the proximal small bowel, but often patients in the immediate postoperative period are very unwell and large volumes of oral contrast medium may be counter productive. However, intravenous contrast medium is necessary and images are obtained in the porto-venous phase at 65 s post-injection of 100 ml 300 mg I/ml iodinated contrast medium. The imaging field is set to extend from the diaphragm to symphysis pubis. The pelvis is included as occasionally sepsis can track from the surgical site in the upper abdomen.
Normal CT appearances Drains Surgical drains are not always left in situ, and there is some controversy in the surgical literature concerning their necessity. However, both volume and amylase content of drain fluid may be of some help in the early diagnosis of an anastomotic leak.3,4 In addition to these drains a fine pancreatic catheter is sometimes left running in the pancreatic duct, through the pancreatic anastomosis and out via the anterior abdominal wall. This can protect the anastomosis, but the use of this manoeuvre is not universal. The drain is usually removed at around 2 weeks.
Computed tomography after radical pancreaticoduodenectomy
Pancreaticogastric versus pancreaticojejunal anastomosis The pancreatic anastomosis can be sutured end to side to the posterior stomach. Some surgeons prefer an anastomosis to the afferent limb of the jejunal loop, and there is evidence that that this decreases the incidence of leaks as a technically better anastomosis can often be achieved. These different techniques can be visualized using CT (Fig. 2b, c). As both this and the biliary anastomosis tend to be hand sewn a suture line is usually not directly visualized. Automated staple devices using easily identifiable metallic staples are frequently used for the gastrojejunostomy.
General postoperative CT findings In a retrospective study, Mortele et al.5 found scanty free fluid and stranding in the retroperitoneal fat to be the most common finding, in 50% patients (Fig. 2a). Thirty three percent of patients in this series of 43 Whipple’s procedures had transient focal fluid collections.5 These are most common in the pancreatic bed, Morrison’s pouch, the right paracolic gutter, and at the level of the anastomosis. Typically these are thin walled or poorly delineated (Fig. 2e). CT alone is unable to differentiate transient, simple, reactive fluid from an infected collection. Percutaneous aspiration is advisable if the patient is clinically septic. Cuffing of the mesenteric vessels is another common postoperative finding and is presumably due to inflammatory or fibrotic change. This, together with small volume lymphadenopathy is a common pattern of local disease recurrence, and care has to be taken when interpreting these appearances. If available, comparison with old investigations is helpful. As with all abdominal surgery, free gas is a common finding. The volume is highly variable and gas can persist for some time. There is lack of consistency in the literature, but one review showed postoperative gas to have cleared in all patients at 18 days post-surgery.6 Therefore, the presence of gas should be interpreted in light of other clinical factors. Aerobilia is another normal, but highly variable, finding and present in around 70% of cases. It is often more common in the left intra-hepatic ducts5 (Fig. 3). The jejunal loop can have a confusing appearance, and it is important not to mistake the fluidfilled or collapsed jejunal loop for a postoperative collection (Fig. 2a, d and g). This loop can usually be identified because of the presence of valvulae
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conniventes, but when these are not obvious, unopacifed small bowel loops can be easily mistaken for lymph node masses or complex collections. If used, oral contrast medium fills the loop with variable frequency. Bluemke et al.7 reported filling in 44% patients, where Mortele et al.5 found useful opacification in only 18%. The use of glucagon has been suggested to aid filling of the afferent loop, but results are inconsistent and its use is not widespread.8 Biliary contrast agents are also advocated by some groups. Strumpp et al.9 found that afferent loop opacification occurred in 95% patients after biliary contrast agent administration. Local experience suggests that the higher spatial resolution of MDCT is helpful in distinguishing bowel from other structures even in the absence of luminal contrast. Other bowel loops, besides the jejunostomy, can migrate up to the hepatic porta. This is often seen in patients with a retrocolic anastomosis where small bowel can migrate through the transverse mesocolon.10 Other normal postoperative findings include mild intra-hepatic duct dilatation (30%) and, less commonly, liver steatosis.5
Complications In a review of 279 patients Miedema et al.11 found a postoperative mortality of 4%. Significant morbidity occurred in 46% with the common complications being delayed gastric emptying (23%), pancreaticojejunal leak (17%), sepsis (10%), biliary leak (9%), gastrointestinal tract bleeding (5%), and intra-abdominal haemorrhage (3%). All complications are more frequent in the elderly and in those patients with a prolonged surgery time and highvolume intraoperative blood loss.11 Early diagnosis of complications is vital. Reoperation is one factor associated with a poorer long-term outcome. Where possible, early radiological intervention, therefore, has a pivotal role and has been shown to improve recovery times and morbidity.2,12,13 Delayed gastric emptying is manifested by distension of the gastric remnant (Fig. 3). Oral contrast studies may be needed to differentiate a mechanical obstruction from an ileus.2 Gastroparesis may be transient, but motility-enhancing agents are often of benefit.
Anastomotic leak Anastomotic leak usually occurs in the first 1e2 weeks after surgery. Any of the anastomoses can fail, but the pancreaticoenterostomy is probably the most important because of the potential leakage of pancreatic secretions into
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S.L. Smith et al.
Figure 2 Normal postoperative appearances. (a) A 53-year-old male patient 5 days post-Whipple’s operation. Rather ill-defined cuffing (short arrow) of the mesenteric vessels and mild oedema of the intra-abdominal fat. Note normal fluid filled jejunostomy loop (long arrow). (b) A 67-year-old female patient 3 months post-Whipple’s operation. Normal appearances of a pancreaticogastric anastomosis (arrow) with pancreatic duct stent. (c) A 74-year-old male patient 6 months post-Whipple’s operation. Normal appearances of a pancreaticojejunal anastomosis (arrow) with pancreatic duct stent. (d) A 47-year-old female patient 10 days post-Whipple’s operation. Normal unopacified jejunal loops in the hepatic porta (arrows). Normal plicae are just visible. Subtle density differences suggest luminal fluid. These appearances should not be confused with a collection or recurrent disease. (e) A 72-year-old male patient 5 days post-Whipple’s operation. Transient, thin-walled peripancreatic fluid collection (arrows). Because of raised inflammatory markers a fine-needle aspiration was performed yielding sterile serous fluid. The collection resolved spontaneously. (f) A 42-year-old female patient 7 days post-Whipple’s operation. Transient abnormal liver parenchymal enhancement involving the lateral segment of the left lobe (arrows). This is probably due transient disruption of portal or hepatic arterial flow. Subsequent follow-up CT showed the liver had returned to normal. (g) A 75-year-old male patient 14 days post-Whipple’s procedure. Investigation performed because of abdominal bloating and poor postoperative progress. Thick slab oblique coronal reformatted images. Normal jejunostomy loop (long arrow), small fluid collection in the pancreatic bed (short arrow) normal at this stage post-surgery. Note distended residue filled stomach suggesting delayed gastric emptying.
Computed tomography after radical pancreaticoduodenectomy
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normal, but complex or gas-containing areas should be viewed with a high index of suspicion (Fig. 4a, b).
Vascular complications Transient perfusion abnormalities within the liver are commonly seen and these usually resolve on follow-up imaging (Fig. 2f). Vascular complications are rare, but include hepatic artery injury, portal vein thrombosis, organ ischaemia, and splenic infarction. CT angiographic studies can be useful in the detection of acute vascular complications, but often fresh blood along with its site of origin are obvious on a standard postoperative study (Figs. 5 and 6). Previous upper gastrointestinal Figure 3 A 48-year-old male patient 7 days postWhipple’s operation showing gastric dilatation. This settled with conservative management. Note areobila and moderate intra-hepatic duct dilatation (arrow).
the abdomen. This complication tends to be more common with small ampullary tumours that have not obstructed the pancreatic duct. With larger tumours it is technically easier to fashion the pancreaticoenterostomy because the pancreatic duct is dilated and, therefore, easier to manipulate. There also tends to be a degree of pancreatic capsular thickening, probably due to low-grade inflammation, which further assists when anastamosing the pancreas to the bowel. A definitive diagnosis of anastomotic failure is not possible using CT unless a direct leak of either oral or biliary contrast medium is demonstrated. However, certain findings coupled with clinical indices can be suggestive. An increase in the amount of free gas, the development of perianastomotic fluid and ascites should suggest the diagnosis. When possible, anastomotic leaks tend to be managed conservatively with percutaneous drainage of any associated fluid collections. Sometimes percutaneous puncture of the intrahepatic bile ducts and stenting of the biliary anastomosis is necessary, but this can be difficult as the ducts are usually not dilated. Complete anastomotic breakdown often necessitates reoperation, which carries a high morbidity and mortality.
Abscess Focal septic collections can occur anywhere in the abdomen and pelvis. Common sites are in the surgical bed and subphrenic spaces. In the context of sepsis any suspicious fluid collection should be aspirated under CT or US control and, if necessary, a drain placed. Simple fluid collections can be
Figure 4 (a) A 78-year-old female patient with postoperative pancreatic bed collection. Gas locules are present (arrows). The patient had raised inflammatory markers and swinging pyrexia. An initial fine-needle aspiration yielded pus. A pigtail drain was inserted under CT control and the collection drained to dryness (b). No further intervention was required.
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Figure 5 A 65-year-old male patient. CT performed at day 5 post-Whipple’s operation after drop in haemoglobin and episode of hypotension. Images show high-density material with the gastric lumen (arrows) consistent with haematoma. At surgery there was bleeding from the gastric anastomosis, which was oversewn.
surgery can increase the incidence of vascular complications, particularly where vascular supply has been interrupted (Fig. 7).
Other complications Radiologists should be alert to other potential postoperative complications, such as Clostridium difficile colitis, wound infection, and complications associated with jejunal feeding. Pancreatitis of the pancreatic remnant is also occasionally seen.
Figure 6 Postoperative CT in a 40-year-old patient 10 days post-Whipple’s procedure. Sudden decompensation and severe abdominal pain. CT shows a flame-shaped area of mesenteric haemorrhage just anterior to the superior mesenteric vessels. High-density collection in the left paracolic space consistent with blood product (arrow). Urgent exploration revealed a mesenteric vein tear. This was repaired.
S.L. Smith et al.
Figure 7 A 63-year-old man 7 days post-Whipple’s procedure for pancreatic head carcinoma. Previous highly selective vagotomy for peptic ulcer disease. Worsening sepsis. Initial CT at 3 days was normal. Repeat CT shows air in the gastric wall (arrows) extending out into the fat of the abdominal cavity. At surgery gastric wall ischaemia with patchy necrosis was found. It was presumed that the gastric vascular supply was compromised because of the previous surgery.
Late complications Recurrence Given the nature of the tumour, recurrence is unfortunately common. In their series Mortele et al.5 found recurrence in 47% of patients. Pancreatic cancer can recur locally in the pancreatic bed or at metastatic sites, usually the liver or lung. They found an overall accuracy of single-section spiral CT of 93.5% for the detection of disease recurrence. At our institution postoperative imaging is not performed routinely. Follow-up is based upon clinical findings and assessment of serum Ca19.9, which is a tumour marker frequently raised in pancreatic-biliary malignancy. A rise in this marker has been shown to occur before clinical or radiological signs develop.14e16 CA 19-9 does have limitations and, for example, in a review of 17 patients with CT evidence of disease recurrence, no rise in the marker was seen in 10 patients.7 A positive resection margin is associated with rapid local recurrence. Bluemke et al.17 found that patients with incomplete resection had a mean time to recurrence of 72 days as compared with 267 days in those with negative margins; however, numbers in the former group were rather small. Interestingly, no significant difference was seen between node-positive and node-negative groups,
Computed tomography after radical pancreaticoduodenectomy
presumably because extensive nodal clearance was performed in both groups.17 Recurrence usually presents as abnormal soft-tissue material related to the surgical site or cuffing retroperitoneal vascular structures (Fig. 8a, b). Care has to taken as a degree of cuffing is normally seen after surgery and particularly where postoperative radiotherapy has been given. However, the nature of the cuffing tends to be different with disease recurrence with continuous, well-defined thickening of the fascial planes around the vessels.18 Serial CT studies may be
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necessary to confirm or refute a local recurrence. The development of ascites more than 30 days post-surgery is an ominous sign with all patients in one typical series having recurrent disease.5 Liver metastases generally appear as rounded hypodense masses best visualized in the portovenous phase of enhancement.
Conclusion Radical pancreaticoduodenectomy is currently the only curative treatment for periampullary malignancies. Surgery is complex and postoperative complications are common. It is important that radiologists are familiar with both the range of normal post-surgical findings and the early and late complications that can occur. Early radiological intervention has an important role in the postoperative period.
Acknowledgements The authors thank Paul Flemming, Simon Girling and Shona Lee, CT Radiographers, for their help in the production of this paper.
References
Figure 8 (a) A 62-year-old male patient 6 months postWhipple’s procedure. Represented with abdominal pain and elevated serum CA19-9. CT shows recurrent tumour in the region of the excised pancreatic head with cuffing of the superior mesenteric artery (arrow). (b) A 70-yearold male patient 8 months post-Whipple’s procedure. Represented with abdominal pain. CT shows diffuse tumour recurrence with encasement of the coeliac trunk branches (arrow) and dilatation of the jejunal loop in keeping with obstruction.
1. Ries LAG, Ksary CL, Hankey BF, et al. SEER cancer statisitics review, 1973e1996. Bethseda: MD:National Cancer Institute; 1999. 2. Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications and outcomes. Ann Surg 1997;226:248e60. 3. Heslin MJ, Harrison LE, Brooks AD, et al. Is intraabdominal drainage necessary after pancreaticoduodenectomy. J Gastrointest Surg 1998;2:373e8. 4. Shinchi H, Wada K, Traverso LW. The usefulness of drain data to identify a clinically relevant pancreatic anastomotic leak after pancreaticoduodenectomy? J Gastrointest Surg 2006;10:490e8. 5. Mortele KJ, Lemmerling M, de Hemptinne B, et al. Postoperative findings following the Whipple procedure: determination of prevalence and morphologic abdominal CT features. Eur Radiol 2000;10:123e8. 6. Gayer G, Jonas T, Apter S, et al. Postoperative pneumoperitoneum as detected by CT: prevalence, duration and relevant factors affecting its possible significance. Abdom Imaging 2000;25:301e5. 7. Bluemke DA, Fishman EK, Kuhlman J. CT Evaluation following Whipple procedure: potential pitfalls in interpretation. J Comput Assist Tomogr 1992;16:705e8. 8. Heiken JP, Balfe DM, Picus D, et al. Radical pancreatectomy postoperative evaluation by CT. Radiology 1984;153:211e5. 9. Strumpp P, Kloppel R, Kahn T. Imaging after a Whipple operation. J Comput Assist Tomogr 2005;29:394e400. 10. Coombs RJ, Zeiss J, Howard JM, et al. CT of the abdomen after the Whipple procedure: value in depicting postoperative anatomy, surgical complications and tumour recurrence. AJR Am J Roentgenol 1990;154:1011e4.
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11. Miedema BW, Sarr MG, van Heerden JA, et al. Complications following pancreaticoduodenectomy. Current management. Arch Surg 1992;127:945e9. 12. Yeo CJ, Cameron JL, Sohn TA, et al. Periampullary adenocarcinoma: analysis of 5 yr survivors. Ann Surg 1998; 227:821e31. 13. Sohn TA, Yeo CJ, Cameron JL, et al. Pancreaticoduodenectomy: role of interventional radiologists in managing patients and complications. J Gastrointest Surg 2003;7:209e19. 14. Glenn J, Sternberg WM, Kurtzman SH, et al. Evaluation of the utility of a radioimmunoassay for serum CA 19-9 levels in patients before and after treatment of carcinoma of the pancreas. J Clin Oncol 1988;6:462e8.
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15. Sperti C, Pasquali C, Catalini S, et al. CA 19-9 as a prognostic index after resection for pancreatic cancer. J Surg Oncol 1993;52:137e41. 16. Beretta E, Malesci A, Zerbi A, et al. Serum CA 19-9 in the post-surgical follow-up of patients with pancreatic cancer. Cancer 1987;60:2428e31. 17. Bluemke DA, Abrams RA, Yeo CJ, et al. Recurrent pancreatic adenocarcinoma: spiral CT evaluation following the Whipple procedure. RadioGraphics 1997;17:303e13. 18. Lepanto L, Gianfelice D, Dery R, et al. Post operative changes, complications and recurrent disease after Whipple’s operation: CT features. AJR Am J Roentgenol 1994; 163:841e6.
PICTORIAL REVIEW
Computed tomography after radical pancreaticoduodenectomy (Whipple’s procedure) S.L. Smitha,*, F. Hampsonb, M. Duxburyc, D.M. Raed, M.T. Sinclaird Departments of aRadiology, and dPancreaticobiliary surgery, Ipswich Hospital, Ipswich, IP4 5PD, UK, b Department of Radiology, Addenbrooke’s Hospital NHS Trust, Cambridge, UK, cDepartment of Surgery, Royal Infirmary of Edinburgh, Little France, Edinburgh EH16 4SU, UK Received 31 July 2007; received in revised form 24 September 2007; accepted 8 October 2007
Whipple’s procedure (radical pancreaticoduodenectomy) is currently the only curative option for patients with periampullary malignancy. The surgery is highly complex and involves multiple anastomoses. Complications are common and can lead to significant postoperative morbidity. Early detection and treatment of complications is vital, and highquality multidetector computed tomography (MDCT) is currently the best method of investigation. This review outlines the surgical technique and illustrates the range of normal postoperative appearances together with the common complications. ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Pancreatic cancer is the fourth leading cause of death due to malignant disease in adults.1 The disease is usually either locally advanced or metastatic at presentation, and less than 20% of patients have disease confined to the pancreas. In this group radical surgery offers the only realistic chance of cure. Classical pancreaticoduodenectomy (Whipple’s procedure) involves complex and aggressive surgery. In the best hands the procedure caries a 1e5% mortality and outcomes have improved in centres that undertake large numbers of resections. Despite the improved mortality statistics there remains a significant postoperative morbidity, estimated to be between 20e30%. In one large series of 650 pancreaticoduodenectomies, a postoperative complication rate of 41e47% was reported.2 Even in those with technically successful surgery the 5-year * Guarantor and correspondent: S.L. Smith, Department of Radiology, Ipswich Hospital, Ipswich, IP4 5PD, UK. Tel.: þ44 1473 703380; fax: þ44 1473 270655. E-mail address: [email protected] (S.L. Smith).
survival for those patients with pancreatic head carcinoma is less than 5%, with the majority of deaths occurring because of recurrent disease. The outcome for other periampullary tumours, namely distal duct cholangiocarcinoma and ampullary carcinoma, is better, reflecting the less locally aggressive nature of these malignancies. Both the early detection of postoperative complications and identification of later disease recurrence are vital. Radiology and, in particular, high-quality multidetector computed tomography (MDCT) studies have a pivotal role here. The aim of the present review is to illustrate normal postoperative CT appearances, as well as complications seen after surgery.
Whipple’s procedure Pancreaticoduodenectomy is indicated primarily for two conditions: tumour in the periampullary region (cancer in the head of pancreas, the ampulla of Vater, the distal bile duct, and the duodenum) and chronic pancreatitis involving the head and uncinate process of the pancreas.
0009-9260/$ - see front matter ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2007.10.012
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Using a rooftop or bilateral subcostal incision, an extensive Kocher manoeuvre is performed to mobilize the duodenum and head of pancreas from the inferior vena cava and aorta. The transverse mesocolon is mobilized from the head and uncinate process of the pancreas to expose the superior mesenteric vein, which is traced to the neck of the pancreas. The dissection is continued to expose the plane between the pancreas and the superior mesenteric and portal veins. The extensive mobilization of the head of pancreas is important to determine the extent of tumour spread to adjacent structures, and hence its resectability. The gallbladder is excised and the common duct is divided to expose the portal vein. The lesser curve of the stomach is prepared for transection. A window is created above the incisura after dividing the branches of the left gastric artery. The greater omentum is divided and an area on the greater curvature of the stomach is prepared by division of the gastroepiploic vessels. The stomach is transected with a linear stapler. The antrum of the stomach is rotated to the right to expose the head and neck of the pancreas. The gastroduodenal artery is exposed and divided. The pancreatic neck is then divided. The ligament of Treitz is mobilized and the jejunum is divided with a linear stapler. The proximal jejunum is passed behind the superior mesenteric vessels to the patient’s right. This helps the dissection of the uncinate process from the superior mesenteric vein. Multiple vessels between the uncinate process and the superior mesenteric vessels are ligated. The resected specimen consists of the gallbladder, the distal common bile duct, duodenum, and proximal jejunum, and the head, neck and uncinate process of the pancreas. Surgical reconstruction consists of a pancreaticoenterostomy, a choledochojejunostomy, and a gastrojejunostomy. A pancreaticoenterostomy can be performed by mucosa-to-mucosa anastomosis with the jejunum or the posterior wall of the stomach. A pancreatic duct stent is usually inserted across the anastomosis using an 8 F infant feeding tube. The choledochojejunostomy is performed by an end-to-side anastomosis. Finally, a retrocolic gastrojejunostomy is performed on the posterior wall of the stomach near its greater curvature (Fig. 1). A drain is placed near the pancreaticoenterostomy and a feeding jejunostomy is performed.
Postoperative CT technique CT is usually performed in the immediate postoperative period because of persistent pyrexia, raised inflammatory markers, or abnormal serum
S.L. Smith et al.
Figure 1 Schematic of standard Whipple’s operation. Anastomoses/suture lines: (A) choledochojejunostomy, (B) pancreaticojejunostomy, (C) gastrojejunostomy, (D) sutured proximal limb of jejunostomy.
bilirubin. Imaging parameters should be adjusted to ensure fine detector collimation (ideally 1 mm section thickness) to facilitate multiplanar reconstructions. At our institution a pragmatic approach to oral contrast medium is used. If relatively healthy, patients receive 700 ml 2% Gastrograffin (Schering Health Care Ltd, Burgess Hill, West Sussex, UK) 30 min before the procedure. It is important to attempt to fill the proximal small bowel, but often patients in the immediate postoperative period are very unwell and large volumes of oral contrast medium may be counter productive. However, intravenous contrast medium is necessary and images are obtained in the porto-venous phase at 65 s post-injection of 100 ml 300 mg I/ml iodinated contrast medium. The imaging field is set to extend from the diaphragm to symphysis pubis. The pelvis is included as occasionally sepsis can track from the surgical site in the upper abdomen.
Normal CT appearances Drains Surgical drains are not always left in situ, and there is some controversy in the surgical literature concerning their necessity. However, both volume and amylase content of drain fluid may be of some help in the early diagnosis of an anastomotic leak.3,4 In addition to these drains a fine pancreatic catheter is sometimes left running in the pancreatic duct, through the pancreatic anastomosis and out via the anterior abdominal wall. This can protect the anastomosis, but the use of this manoeuvre is not universal. The drain is usually removed at around 2 weeks.
Computed tomography after radical pancreaticoduodenectomy
Pancreaticogastric versus pancreaticojejunal anastomosis The pancreatic anastomosis can be sutured end to side to the posterior stomach. Some surgeons prefer an anastomosis to the afferent limb of the jejunal loop, and there is evidence that that this decreases the incidence of leaks as a technically better anastomosis can often be achieved. These different techniques can be visualized using CT (Fig. 2b, c). As both this and the biliary anastomosis tend to be hand sewn a suture line is usually not directly visualized. Automated staple devices using easily identifiable metallic staples are frequently used for the gastrojejunostomy.
General postoperative CT findings In a retrospective study, Mortele et al.5 found scanty free fluid and stranding in the retroperitoneal fat to be the most common finding, in 50% patients (Fig. 2a). Thirty three percent of patients in this series of 43 Whipple’s procedures had transient focal fluid collections.5 These are most common in the pancreatic bed, Morrison’s pouch, the right paracolic gutter, and at the level of the anastomosis. Typically these are thin walled or poorly delineated (Fig. 2e). CT alone is unable to differentiate transient, simple, reactive fluid from an infected collection. Percutaneous aspiration is advisable if the patient is clinically septic. Cuffing of the mesenteric vessels is another common postoperative finding and is presumably due to inflammatory or fibrotic change. This, together with small volume lymphadenopathy is a common pattern of local disease recurrence, and care has to be taken when interpreting these appearances. If available, comparison with old investigations is helpful. As with all abdominal surgery, free gas is a common finding. The volume is highly variable and gas can persist for some time. There is lack of consistency in the literature, but one review showed postoperative gas to have cleared in all patients at 18 days post-surgery.6 Therefore, the presence of gas should be interpreted in light of other clinical factors. Aerobilia is another normal, but highly variable, finding and present in around 70% of cases. It is often more common in the left intra-hepatic ducts5 (Fig. 3). The jejunal loop can have a confusing appearance, and it is important not to mistake the fluidfilled or collapsed jejunal loop for a postoperative collection (Fig. 2a, d and g). This loop can usually be identified because of the presence of valvulae
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conniventes, but when these are not obvious, unopacifed small bowel loops can be easily mistaken for lymph node masses or complex collections. If used, oral contrast medium fills the loop with variable frequency. Bluemke et al.7 reported filling in 44% patients, where Mortele et al.5 found useful opacification in only 18%. The use of glucagon has been suggested to aid filling of the afferent loop, but results are inconsistent and its use is not widespread.8 Biliary contrast agents are also advocated by some groups. Strumpp et al.9 found that afferent loop opacification occurred in 95% patients after biliary contrast agent administration. Local experience suggests that the higher spatial resolution of MDCT is helpful in distinguishing bowel from other structures even in the absence of luminal contrast. Other bowel loops, besides the jejunostomy, can migrate up to the hepatic porta. This is often seen in patients with a retrocolic anastomosis where small bowel can migrate through the transverse mesocolon.10 Other normal postoperative findings include mild intra-hepatic duct dilatation (30%) and, less commonly, liver steatosis.5
Complications In a review of 279 patients Miedema et al.11 found a postoperative mortality of 4%. Significant morbidity occurred in 46% with the common complications being delayed gastric emptying (23%), pancreaticojejunal leak (17%), sepsis (10%), biliary leak (9%), gastrointestinal tract bleeding (5%), and intra-abdominal haemorrhage (3%). All complications are more frequent in the elderly and in those patients with a prolonged surgery time and highvolume intraoperative blood loss.11 Early diagnosis of complications is vital. Reoperation is one factor associated with a poorer long-term outcome. Where possible, early radiological intervention, therefore, has a pivotal role and has been shown to improve recovery times and morbidity.2,12,13 Delayed gastric emptying is manifested by distension of the gastric remnant (Fig. 3). Oral contrast studies may be needed to differentiate a mechanical obstruction from an ileus.2 Gastroparesis may be transient, but motility-enhancing agents are often of benefit.
Anastomotic leak Anastomotic leak usually occurs in the first 1e2 weeks after surgery. Any of the anastomoses can fail, but the pancreaticoenterostomy is probably the most important because of the potential leakage of pancreatic secretions into
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Figure 2 Normal postoperative appearances. (a) A 53-year-old male patient 5 days post-Whipple’s operation. Rather ill-defined cuffing (short arrow) of the mesenteric vessels and mild oedema of the intra-abdominal fat. Note normal fluid filled jejunostomy loop (long arrow). (b) A 67-year-old female patient 3 months post-Whipple’s operation. Normal appearances of a pancreaticogastric anastomosis (arrow) with pancreatic duct stent. (c) A 74-year-old male patient 6 months post-Whipple’s operation. Normal appearances of a pancreaticojejunal anastomosis (arrow) with pancreatic duct stent. (d) A 47-year-old female patient 10 days post-Whipple’s operation. Normal unopacified jejunal loops in the hepatic porta (arrows). Normal plicae are just visible. Subtle density differences suggest luminal fluid. These appearances should not be confused with a collection or recurrent disease. (e) A 72-year-old male patient 5 days post-Whipple’s operation. Transient, thin-walled peripancreatic fluid collection (arrows). Because of raised inflammatory markers a fine-needle aspiration was performed yielding sterile serous fluid. The collection resolved spontaneously. (f) A 42-year-old female patient 7 days post-Whipple’s operation. Transient abnormal liver parenchymal enhancement involving the lateral segment of the left lobe (arrows). This is probably due transient disruption of portal or hepatic arterial flow. Subsequent follow-up CT showed the liver had returned to normal. (g) A 75-year-old male patient 14 days post-Whipple’s procedure. Investigation performed because of abdominal bloating and poor postoperative progress. Thick slab oblique coronal reformatted images. Normal jejunostomy loop (long arrow), small fluid collection in the pancreatic bed (short arrow) normal at this stage post-surgery. Note distended residue filled stomach suggesting delayed gastric emptying.
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normal, but complex or gas-containing areas should be viewed with a high index of suspicion (Fig. 4a, b).
Vascular complications Transient perfusion abnormalities within the liver are commonly seen and these usually resolve on follow-up imaging (Fig. 2f). Vascular complications are rare, but include hepatic artery injury, portal vein thrombosis, organ ischaemia, and splenic infarction. CT angiographic studies can be useful in the detection of acute vascular complications, but often fresh blood along with its site of origin are obvious on a standard postoperative study (Figs. 5 and 6). Previous upper gastrointestinal Figure 3 A 48-year-old male patient 7 days postWhipple’s operation showing gastric dilatation. This settled with conservative management. Note areobila and moderate intra-hepatic duct dilatation (arrow).
the abdomen. This complication tends to be more common with small ampullary tumours that have not obstructed the pancreatic duct. With larger tumours it is technically easier to fashion the pancreaticoenterostomy because the pancreatic duct is dilated and, therefore, easier to manipulate. There also tends to be a degree of pancreatic capsular thickening, probably due to low-grade inflammation, which further assists when anastamosing the pancreas to the bowel. A definitive diagnosis of anastomotic failure is not possible using CT unless a direct leak of either oral or biliary contrast medium is demonstrated. However, certain findings coupled with clinical indices can be suggestive. An increase in the amount of free gas, the development of perianastomotic fluid and ascites should suggest the diagnosis. When possible, anastomotic leaks tend to be managed conservatively with percutaneous drainage of any associated fluid collections. Sometimes percutaneous puncture of the intrahepatic bile ducts and stenting of the biliary anastomosis is necessary, but this can be difficult as the ducts are usually not dilated. Complete anastomotic breakdown often necessitates reoperation, which carries a high morbidity and mortality.
Abscess Focal septic collections can occur anywhere in the abdomen and pelvis. Common sites are in the surgical bed and subphrenic spaces. In the context of sepsis any suspicious fluid collection should be aspirated under CT or US control and, if necessary, a drain placed. Simple fluid collections can be
Figure 4 (a) A 78-year-old female patient with postoperative pancreatic bed collection. Gas locules are present (arrows). The patient had raised inflammatory markers and swinging pyrexia. An initial fine-needle aspiration yielded pus. A pigtail drain was inserted under CT control and the collection drained to dryness (b). No further intervention was required.
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Figure 5 A 65-year-old male patient. CT performed at day 5 post-Whipple’s operation after drop in haemoglobin and episode of hypotension. Images show high-density material with the gastric lumen (arrows) consistent with haematoma. At surgery there was bleeding from the gastric anastomosis, which was oversewn.
surgery can increase the incidence of vascular complications, particularly where vascular supply has been interrupted (Fig. 7).
Other complications Radiologists should be alert to other potential postoperative complications, such as Clostridium difficile colitis, wound infection, and complications associated with jejunal feeding. Pancreatitis of the pancreatic remnant is also occasionally seen.
Figure 6 Postoperative CT in a 40-year-old patient 10 days post-Whipple’s procedure. Sudden decompensation and severe abdominal pain. CT shows a flame-shaped area of mesenteric haemorrhage just anterior to the superior mesenteric vessels. High-density collection in the left paracolic space consistent with blood product (arrow). Urgent exploration revealed a mesenteric vein tear. This was repaired.
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Figure 7 A 63-year-old man 7 days post-Whipple’s procedure for pancreatic head carcinoma. Previous highly selective vagotomy for peptic ulcer disease. Worsening sepsis. Initial CT at 3 days was normal. Repeat CT shows air in the gastric wall (arrows) extending out into the fat of the abdominal cavity. At surgery gastric wall ischaemia with patchy necrosis was found. It was presumed that the gastric vascular supply was compromised because of the previous surgery.
Late complications Recurrence Given the nature of the tumour, recurrence is unfortunately common. In their series Mortele et al.5 found recurrence in 47% of patients. Pancreatic cancer can recur locally in the pancreatic bed or at metastatic sites, usually the liver or lung. They found an overall accuracy of single-section spiral CT of 93.5% for the detection of disease recurrence. At our institution postoperative imaging is not performed routinely. Follow-up is based upon clinical findings and assessment of serum Ca19.9, which is a tumour marker frequently raised in pancreatic-biliary malignancy. A rise in this marker has been shown to occur before clinical or radiological signs develop.14e16 CA 19-9 does have limitations and, for example, in a review of 17 patients with CT evidence of disease recurrence, no rise in the marker was seen in 10 patients.7 A positive resection margin is associated with rapid local recurrence. Bluemke et al.17 found that patients with incomplete resection had a mean time to recurrence of 72 days as compared with 267 days in those with negative margins; however, numbers in the former group were rather small. Interestingly, no significant difference was seen between node-positive and node-negative groups,
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presumably because extensive nodal clearance was performed in both groups.17 Recurrence usually presents as abnormal soft-tissue material related to the surgical site or cuffing retroperitoneal vascular structures (Fig. 8a, b). Care has to taken as a degree of cuffing is normally seen after surgery and particularly where postoperative radiotherapy has been given. However, the nature of the cuffing tends to be different with disease recurrence with continuous, well-defined thickening of the fascial planes around the vessels.18 Serial CT studies may be
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necessary to confirm or refute a local recurrence. The development of ascites more than 30 days post-surgery is an ominous sign with all patients in one typical series having recurrent disease.5 Liver metastases generally appear as rounded hypodense masses best visualized in the portovenous phase of enhancement.
Conclusion Radical pancreaticoduodenectomy is currently the only curative treatment for periampullary malignancies. Surgery is complex and postoperative complications are common. It is important that radiologists are familiar with both the range of normal post-surgical findings and the early and late complications that can occur. Early radiological intervention has an important role in the postoperative period.
Acknowledgements The authors thank Paul Flemming, Simon Girling and Shona Lee, CT Radiographers, for their help in the production of this paper.
References
Figure 8 (a) A 62-year-old male patient 6 months postWhipple’s procedure. Represented with abdominal pain and elevated serum CA19-9. CT shows recurrent tumour in the region of the excised pancreatic head with cuffing of the superior mesenteric artery (arrow). (b) A 70-yearold male patient 8 months post-Whipple’s procedure. Represented with abdominal pain. CT shows diffuse tumour recurrence with encasement of the coeliac trunk branches (arrow) and dilatation of the jejunal loop in keeping with obstruction.
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