Pancreaticoduodenectomy represents a major surgery for tumors located at the pancreatic head and the ampullary/periampullary region. This complex procedure is associated with a high morbidity rate. Many surgical techniques have been proposed in order to reduce mortality rates, although post-procedure complications represent a current problem. Different imaging findings and complications may appear depending on the surgical technique used. Hence, radiologists should be familiarized with them to distinguish normal findings from real complications. The most challenging scenarios are represented by abdominal fluid collections, and tumor recurrence, that may frequently mimic normal postsurgical changes.
Hinweise
The aim of this paper is to describe these different findings and provide keys to recognize them correctly.
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Abkürzungen
BF
Biliary fistula
DGE
Delayed gastric emptying
DJ
Duodenojejunostomy
DWI
Diffusion-weighted imaging
GJ
Gastrojejunostomy
MDCT
Multi-detector computed tomography
MRCP
Magnetic resonance cholangiopancreatography
MRI
Magnetic resonance imaging
PF
Pancreatic fistula
PG
Pancreaticogastrostomy
PJ
Pancreaticojejunostomy
Key points
MDCT represents the first-line imaging modality after pancreaticoduodenectomy.
Most challenging complication diagnoses are pancreatic fistula and tumor recurrency.
Additional angiographic-CT phase is recommended when vascular complications are suspected.
MRI with gadoxetic-acid is recommended to detect hepaticojejunostomy stenosis and biliary fistula.
DWI helps differentiate local recurrence form postsurgical changes when CT is inconclusive.
Background
Pancreaticoduodenectomy is a major surgery for tumors located at the pancreatic head and the ampullary/periampullary region, and represents the only curative procedure available to date for this group of diseases. This complex procedure has been associated with a high morbidity rate [1]. Due to surgical techniques improvement, mortality rates have been significantly reduced, although post-procedure complications represent a frequent problem [2]. As there are different surgical techniques, each one with specific post-surgical imaging findings, the radiologist must be familiar with them in order to make a correct diagnosis and guide the patient's follow-up.
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The aim of this article is to review the main pancreatic, gastric and bilioenteric reconstruction techniques used after a pancreaticoduodenectomy, illustrating the normal imaging findings and their complications.
Surgical technique
Pancreaticoduodenectomy consists of two phases: the resection phase that involves the resection of pancreatic head, duodenum, gallbladder, distal bile duct and proximal jejunum, with or without pylorus preservation, followed by the reconstruction phase with the creation of three anastomosis: pancreaticojejunostomy, hepaticojejunostomy, and gastrojejunostomy (Whipple procedure) or duodenojejunostomy [3] (Fig. 1).
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Computed tomography (CT) represents the main imaging modality in postsurgical assessment of pancreaticoduodenectomy due to its capability to explore the whole abdominal cavity with a high spatial resolution and short acquisition time. For routine post-surgical follow-up, we suggest a non-contrast phase to depict high density findings (surgical clips, pancreatic stent, and blood) and a portal venous phase (60–70 s delay) including the pelvis for a global assessment. Positive oral contrast agent is routinely used for postsurgical intestinal anatomy distinction, specially the efferent limb and gastroenteroanastomosis. Protocol should be based on clinical findings during a complicated postoperative period, with an abdomino-pelvic non-contrast phase for hemorrhagic fluid detection and an additional CT-angiographic phase if vascular complication is suspected. In cases of abdominal collection, a late phase after three minutes may improve its distinction. The use of neutral oral agents, such as water, is not recommended as bowel loops may mimic a collection.
In order to improve imaging surveillance quality, magnetic resonance imaging (MRI) should be considered an additional method to CT for several reasons. Firstly, it is well known that MR provides a higher pancreatic and hepaticojejunostomy evaluation, especially when MR cholangiopancreatography (MRCP) or hepatobiliary contrast agents are used [4]. Secondly, MR can better distinguish tumor recurrence from other normal conditions such as collapsed loop, since it better depicts endoluminal content, or perivascular cuffing and other mass-like imaging in the surgical bed based on diffusion weighted imaging (DWI).
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Pancreatic–enteric anastomosis
Pancreatic–enteric anastomosis represents the most challenging anastomosis during the surgical procedure and leads to most post-procedure complications [5]. There are two main pancreatic–enteric anastomosis techniques: pancreaticojejunostomy (PJ) and pancreatic-gastro (PG) anastomosis.
Different metaanalyses show there is no significant difference between PJ and PG anastomosis in terms of pancreatic fistula, mortality or morbidity [6, 7]. Although some authors report a slight reduction in pancreatic fistula development with PG [8]. In our institution, PJ is the most used anastomosis. Different surgical techniques are employed to create the PJ anastomosis; the most important are: duct-to-mucosa and invagination anastomosis, being the former the most frequently used (Figs. 2, 3).
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Hepaticojejunostomy
Hepaticojejunostomy is usually located 20–30 cm distal to PJ. It may be difficult to find due to jejunal limb collapse. Pneumobilia is a normal postoperative finding that helps to identify it, as well as using the hepatic hilum as a landmark (looking for surgical clips). When positive oral contrast agent is used, sometimes reflux to the afferent limb may occur, so it can fill the anastomosis and helps to recognize it. The use of coronal plane reconstructions is recommended for a better visualization. MRCP and MRI with gadoxetic acid are the most useful methods to assess permeability (Fig. 4).
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Gastrojejunostomy
Gastrojejunostomy allows reconstitution of the digestive tract. Depending on the primary pathology and the surgeon's choice, it can be performed with resection of the gastric antrum (classic Whipple procedure) or with pylorus preservation (pylorus preservation procedure). This anastomosis is usually located in the left upper quadrant. The use of a positive oral contrast agent is essential to digestive tract reconstruction assessment, allowing delineation of marked change in mucosal pattern in gastroenteric anastomosis and pylorus identification, when preserved (Fig. 5).
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Intestinal reconstruction
Classic procedure includes intestinal reconstruction by an unique jejunal loop where the three anastomoses are performed. This technique is known as Child type reconstruction. Another popular intestinal reconstruction technique is the Roux-en-Y type, in which a jejunal loop is constructed in order to make the pancreaticojejunal and biliodigestive anastomosis. This jejunal loop is called afferent or biliodigestive limb. In our institution, a Roux variant known as Machado type is used, which allows to reduce morbidity and mortality in case of pancreatic or biliary fistula, preserving each anastomosis separately. Intestinal reconstruction techniques are exposed in Fig. 6.
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Normal postoperative findings and complications
In this section, normal postoperative findings of each anastomosis or intestinal reconstruction technique, as well as their complications will be discussed (Table 1).
Table 1
Normal findings and complications
Normal findings
Complications
Postoperative Anatomy
Surgical techniques
Related Complications
Fluid, edema and fat stranding
Pancreaticojejunostomy
Duct-to-mucosa
Invagination
Use of tutor
Pancreatic Fistula
Stricture
Tutor migration
Perivascular cuffing
Biliary-enteric Anastomosis
Hepaticojejunostomy
Chledochojejunostomy
Biliary fistula (Bilom)
Stricture
Lymph nodes
Efferent limb (Alimentary limb)
Gastrojejunostomy
Duodenojejunostomy
Delayed gastric emptying
Stricture
Pancreatic duct dilatation
Afferent limb (Biliary or Roux limb)
Child
Y de Rox
Afferent limb syndrome
Mild intrahepatic biliary dilatation
Vascular
–
Hemorrhage
Pseudoaneurysm
Hepatic Infarct
Venous thrombosis
Tumor recurrence
Normal postoperative findings
During the early perioperative period, imaging may show temporary findings related to surgery that should not be misunderstood as tumor recurrence or abnormal inflammatory processes. These findings include fluid, edema and peripancreatic fat stranding, pneumoperitoneum, pneumobilia and pneumowirsung, mild pancreatic duct and/or intrahepatic biliary dilatation, lymph nodes and perivascular cuffing (Fig. 7).
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Tumor recurrence mimics: imaging challenge
Normal postoperative findings may mimic tumor recurrence. Lymphadenopathy, collapsed loop, perivascular cuffing and pancreatic and/or intrahepatic ducts dilatation represent the major challenges.
Lymphadenopathy
Lymphadenopathy represents one of the most frequent postoperative findings. Adenopathies are expected to regress within the first six months after surgery, but can sometimes persist for longer periods [9].
Although morphological characteristics such as short axis less than 1cm and oval shape can help identify reactive lymph nodes in the early period, the new-formed or growing nodes should raise suspicion for malignancy [10] (Fig. 8).
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Collapsed loop
Collapsed loops may be difficult to evaluate in CT scans. The mass-like appearance makes it difficult to rule out recurrence (Fig. 9). Multiplanar reconstructions can help by following the loop beyond the surgical bed in many cases. In doubtful cases, MRI can be chosen as an imaging follow-up method to differentiate from tumor recurrence as it can usually determine the fluid content of the loop, thus differentiating it from tumor recurrence (Figs. 10 and 11). For this purpose, we recommend the addition of thin axial and coronal T2 weighted images (3 mm) in order to better depict intestinal folds which are clearly visible in the yeyunal wall of a collapsed loop and absent in case of a recurrence.
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Perivascular cuffing
Perivascular cuffing is characterized by the presence of soft-tissue stranding in mesenteric fat that occurs within the surgical bed and surrounding celiac axis; it is due to a transient inflammatory reaction. It may appear as a mass-like image and can be easily mistaken for residual disease on CT scan (Fig. 12). MRI, especially with the use of DWI, can help differentiate this transient and benign finding from tumor recurrence when CT is inconclusive (Fig.13).
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Pancreatic and/or intrahepatic ducts dilatation
Mild biliary and pancreatic dilatation could be a persistent normal finding. Significant dilatation, or progression of the known one, should raise suspicion of local recurrence near the pancreaticojejunostomy or anastomotic stricture (Fig.14).
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As exposed above, tumor recurrence is a diagnosis challenge. At this point, the use of MRI with DWI improves the differentiation between early local recurrence from post-surgical changes: the presence of mass-like tissue on surgical bed with restriction at DWI with low ADC map values is suggestive of tumor recurrence [11]. MRI has proven to be a highly sensitive method in oncological follow-up, and the correct interpretation of DWI is key to detecting small lesions that are not visible with other imaging methods [12, 13].
At least, it is important to highlight that strict follow-up and combination with serum CA 19-9 is essential to confirm recurrence. If doubt exists after using the imaging modalities we have discussed, 18 FDG PET-CT can help to confirm or dismiss the diagnosis.
Tumor recurrence is the main cause of poor long-term outcome after pancreaticoduodenectomy, so radiologist’s awareness must be elevated: do not forget to use as many prior scans as available, especially the earliest postoperative scan.
Complications
Pancreaticojejunostomy
It is important to recognize the anastomosis type (PG vs PJ), because it is the main site of complications. The most frequent one is pancreatic fistula (PF), with a global incidence of 4 to 30%. It is associated with increased length of hospital stay and mortality [4].
PF is a clinical diagnosis characterized by the presence of amylase concentration three times higher in fluid collection than in serum, and/or persistence of it 7–10 days after surgery. At CT, it appears as a fluid collection near the PJ (Fig. 15).
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When a fluid collection is seen near the PJ, it is important to identify whether it is an infected collection. PF usually is expected to resolve by itself, while an abdominal abscess requires drainage. CT features that suggest abscess include heterogeneity within the collection with or without air content, and the presence of an enhancing wall (Fig. 16). Nevertheless, radiologists should interpret these findings in conjunction with clinical history and laboratory data, because imaging appearance between PF and abscess usually overlap, representing a major challenge [4] (Fig. 17).
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In order to reduce the risk of PF, a stent in the anastomosis may be placed, depending on the surgeon's criteria. Stent migration is a usual finding, with no pathological significance.
Another complication to be aware of is anastomosis stenosis. PJ diameter may be reduced, either due to fibrosis or tumor recurrence. Stenosis predisposes to recurrent pancreatitis episodes, which lead to PJ assessment in order to achieve the etiology (Fig. 18).
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Hepaticojejunostomy
Biliary fistula (BF) is a rare complication of hepaticojejunostomy, occurring in 3–4% of all procedures. The presence of a fluid collection adjacent to the anastomosis is a finding suggestive of BF in CT imaging [14] (Fig. 19).
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As BF and PF depict similar imaging findings, and the proximity of the anastomosis (PJ and HJ) may not confirm the leak origin, biochemical analysis of fluid is essential for correct diagnosis: high bilirubin levels in fluid confirm BF [15] (Fig. 20).
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Stricture is another complication, commonly in late controls. Clinical presentation includes jaundice and cholangitis, in case it is not detected early [16]. As expected, imaging shows intrahepatic biliary tract dilatation. In those cases, tumor recurrence is the main diagnosis to be ruled out, due to treatment and prognosis implications [17] (Fig. 21).
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The use of MRI with hepatobiliary-specific contrast agent (gadoxetic-acid) represents a safe and noninvasive option to detect postoperative biliary complications, such as hepaticojejunostomy stenosis and biliary fistula. Biliary excretion of contrast agent on hepatobiliary late phase (20 min) allows demonstration of anastomosis patency by identifying afferent loop filling or contrast leak into a neighboring fluid collection, allowing diagnosis of a biloma (Fig. 22). Sometimes, further delayed images (2 hours or more) must be acquired to achieve these diagnoses.
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Gastrojejunostomy and intestinal reconstruction
As both gastrojejunostomy and intestinal reconstruction are intended to allow return of digestive tract transit after surgery, they are mentioned together.
Regarding gastrojejunostomy, delayed gastric emptying (DGE) represents a major complication after pancreaticoduodenectomy. Although it is a clinically diagnosed complication, imaging may suggest the diagnosis and dismiss others (Fig. 23). The pylorus-preserving procedure was thought to reduce DGE and avoid the biliary reflux from the afferent limb, improving long-term patient nutritional status. Nevertheless, there is no strong evidence of difference between this procedure and Whipple’s [18]. Anastomotic dehiscence is a rare and life-threatening complication related to gastrojejunostomy (Fig. 24).
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Another clinical scenario may be present when afferent limb is partially or completely obstructed, developing afferent limb syndrome. This syndrome is characterized by mechanical obstruction of afferent limb, may be acute or chronic depending on grade of obstruction. Abdominal pain, nausea, vomiting, bacterial overgrowth, diarrhea, malabsorption and undernutrition are its usual clinical presentation resulting in pancreatobiliary disturb (Fig. 25). It is a frequent complication after Y de Roux reconstruction, described at least in 13% cases [19].
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Vascular complications
Hemorrhagic complications are infrequent (2–15%), with a high mortality rate [20]. They usually develop during the early period after surgery (< 1 week). The inadequate ligation of gastroduodenal artery during surgery is a leading cause of active bleeding. Multiphase CT scan is an excellent method to depict vascular complications: the presence of dense collection on non-contrast CT suggests hematic collection, whereas a dense area seen on arterial phase, which increases in late ones, is consistent with active bleeding [21] (Fig. 26).
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Direct vascular injury either from iatrogenic trauma or vascular erosion due to anastomosis dehiscence may develop pseudoaneurysm, which represents a challenging diagnosis with a high potential mortality rate if untreated (Fig. 27).
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Vascular injury also may determine decreasing blood flow to certain organs with infarct development (Fig. 28).
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Conclusion
The pancreaticoduodenectomy procedure is associated with several postsurgical complications, knowledge of which is essential. Radiologists should be able to depict the principal anatomy landmarks and normal post-procedure findings, as well as imaging findings of each possible complication in order to achieve the correct diagnosis.
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Declarations
Ethics approval and consent to participate
Institutional Review Board approval and written informed consent from all subjects (patients) in this study were obtained.
Consent for publication
Consent to publish was obtained.
Competing interests
The authors of this study have no competing interests.
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