Keywords

Introduction

Magnetic resonance imaging (MRI) of the pancreas has conventionally taken a secondary role in the diagnosis and staging of pancreatic malignancy.

The multidetector computed tomography (MDCT) pancreatic protocol has been extensively validated for the use of pancreatic staging for pancreatic carcinoma [1] and is the mainstay for the diagnosis and evaluation of surgical resectability. This is due to the superior spatial resolution of CT and the ability to multiplanar reformat the images for accurate tumor and vessel assessment.

However, due to its superior soft tissue contrast resolution, MRI has significant advantages over CT in the detection of small noncontour deforming pancreatic lesions, characterization and differentiation between benign and malignant lesions, and the detection and characterization of liver and peritoneal metastasis [2].

With increasing advancement in MRI technology, comparisons between CT and MRI have shown a similar ability in prediction of vessel and tumor involvement [3,4,5].

MRI Technique

The multipulse capability of MRI enables detection and characterization of pancreatic and liver lesions with a high degree of accuracy. Each individual sequence obtained provides tissue specific information of a lesion. The information gathered from all the sequences aids in the characterization of lesions where CT and conventional ultrasound cannot. This is particularly useful when endoscopic ultrasound with fine needle aspiration of the pancreas is not available or cannot be performed.

There are standard sequences used for the assessment of the pancreas, with occasional variations depending on the clinical question, and the age and capability of the MRI scanner available.

The standard sequences are outlined below.

T1 Weighted Gradient Recalled Echo (GRE)

The axial T1 weighted GRE sequence provides excellent delineation of the pancreatic contour demonstrating good anatomical detail. This is due to the inherent high signal of the pancreas on the T1 weighted sequences due to the presence of acinar cells with the pancreas, and the high content of paramagnetic ions such as manganese [6]. The pancreas is clearly outlined against the higher T weighted signal peri-pancreatic fat.

Fat suppressed T1 weighted sequences suppresses the macroscopic fat. The peri-pancreatic fat therefore becomes dark, thus increasing the conspicuity of the inherently high signal pancreas. This sequence is used for the post-contrast scans due to the high lesion contrast [7].

Most pancreatic abnormalities are low signal on the T1 weighted sequence including pancreatic lesions and pancreatitis, and therefore visible within the high signal pancreas. This enables the detection of small lesions (less than 2 cm) which can be beyond the resolution of CT. Difficulty may ensue when there is a pancreatic carcinoma within acute or chronic pancreatitis, as both pathologies return a low T1 weighted signal.

The T1 weighted sequences without fat suppression, where the surrounding peri-pancreatic fat is of higher signal to the pancreas is used to assess tumor infiltration into the fat and adjacent vessels.

T2 Weighted Sequences

On the T2 weighted fast or turbo spin echo (FSE/TSE) sequence, the normal pancreas is not as clearly defined as it has an intermediate signal intensity, only slightly higher than surrounding muscle. Solid pancreatic lesions are of low signal on this sequence making conspicuity with the pancreas difficult.

On fat suppressed images, there is little contrast differentiation between normal pancreas and surrounding peri-pancreatic fat.

However, fluid is bright on T2 weighted sequences. Thus, cystic lesions can be confidently identified within the pancreas, as can the outline of the pancreatic and biliary ductal system.

The presence of necrosis or cystic degeneration of a solid lesion is also more clearly identified on this sequence due to the internal fluid content.

On the T2 weighted sequences, the peri-pancreatic tissue is of a higher signal than the adjacent pancreas. This provides good delineation of the peri-pancreatic fat adjacent to pancreatic contour, enabling assessment of peri-pancreatic inflammation, peri-pancreatic tumor infiltration, and identification of lymph nodes.

Diffusion Weighted Sequences

The diffusion weighted sequence (DWI) is becoming an established sequence for the assessment of the pancreas due to its ability to provide information on the cellular density of tissue.

In normal tissue, water molecules diffuse freely in relation to molecular interactions and the cellular environment (Brownian motion). However, in the presence of pathology, this diffusion is restricted due to changes at the cellular level such as edema, fibrosis, or increased cellular density [8].

The diffusion weighted sequence is sensitive to molecular motion as it applies two “diffusion gradients” around the 180° refocusing pulse. Molecules that are restricted in their movement (due to cellular change) receive both gradient excitations and therefore receive no net change to their phase, and therefore return a high signal. Molecules that are unrestricted in their movement (normal tissue) do not receive both gradients excitations as they are motion, and therefore experience a phase loss and return a low signal.

The timing and application of these diffusion gradients determine the sensitivity to diffusion and is indicated by the use of “b-values,” with increasing b-values indicating increasing sensitivity to diffusion.

A diffusion sequence will routinely begin with a b-factor of “b-0” to establish a baseline image and then with b-values of increasing value tailored to examine a particular tissue type. On images with a high “b” value, there is loss of anatomical detail of the solid organs, resulting in lesions with restricted diffusion appearing conspicuous.

The diffusion sequence in its natural form contains T2 contrast due to the repetition and echo time used in these sequences. The T2 contamination, termed “T2 shine through,” can be misinterpreted as an indication of pathology if not fully understood and recognized. To correct this shine through, the calculation of apparent diffusion coefficients, or “ADC map” as it is better known, is required.

The ADC map is calculated using a logarithmic algorithm involving the b-0 and the second, or the multiple b-values acquired. Through the application of this algorithm, the effects of T2 shine through are removed, leaving a corrected image set. This ADC map is opposite to the initial uncorrected image set in signal properties: areas of restricted diffusion which have a high signal on the uncorrected raw image set will have a low signal on the ADC map [9,10,11]. Quantification can be assessed on the ADC map using regions of interest.

As a result of the varied cellular densities of normal pancreas and pancreatic pathology, DWI can potentially be useful in the identification and characterization of pancreatic lesions.

Dynamic Contrast Scans

Dynamic contrast enhanced T1 weighted fat suppressed gradient recalled echo (GRE) sequences are performed following intravenous gadolinium contrast administration. The contrast enhanced sequences require patient cooperation with at least 4 to 5 breath-holds of at least 11 s in length.

An extracellular gadolinium agent is conventionally used for assessment of the pancreas. This behaves similarly to contrast agents in CT by diffusing rapidly from the intravascular space into the extracellular space. These are excreted by glomerular filtration via the kidneys.

Peak pancreatic parenchymal enhancement occurs at 35 s post-contrast resulting in intense homogenous pancreatic enhancement where lesion conspicuity is at its greatest. The pancreas then becomes isointense to the liver on the portal venous and delayed phases, with loss of contrast enhancement by 3 min. The pancreas is imaged 35 s (pancreatic parenchymal phase), 70 s (portal venous) and delayed phase scans, usually 1 and 3 min.

The contrast enhanced images also provides evaluation of the adjacent vessels for vascular staging.

Magnetic Resonance Cholangiopancreatography (MRCP)

MRCP is a fluid targeted sequence depicting the biliary and pancreatic ductal system. Two types of MRCP technique are utilized.

A thick slab single-shot turbo spin echo T2 sequence can be obtained in any plane with a single short breath hold. This provides an excellent overall view of the entire biliary and pancreatic ductal system.

The multisection thin slab single shot spin echo sequence requires breath-hold and therefore patient cooperation. This sequence provides more detailed view of the pancreatic duct providing thin slice sequential images.

To visualize the biliary tract and pancreatic duct without fluid from the surrounding stomach and duodenum obscuring the view, the patient is starved for at least 4–6 h and given a T2 negative oral contrast agent such as pineapple juice immediately before the scan. This effectively nulls the signal from the stomach and duodenum. On the MRCP sequences, the solid organ detail is not present, providing a clear view of the ductal system such as in ERCP.

The dorsal pancreatic duct is normally 2 to 3 mm in diameter, increasing caliber from the tail of the pancreas to head. Although there are several tiny side branches arising from the pancreatic duct, these are not normally identified on MRCP unless pathologically dilated.

Cystic lesions and ductal abnormalities can clearly be identified on MRCP [12].

The presence of ductal narrowing may indicate the presence of a small pancreatic lesion and may be the only sign visible on imaging. Intraductal filling defects such as stones which are low signal compared to the high signal duct in patients with chronic pancreatitis are also clearly depicted as an alternative cause of ductal dilatation [13].

Secretin MRCP

Dynamic assessment of the pancreatic duct is possible with the administration of the enzyme secretin. This is an amino acid polypeptide hormone which is usually secreted by the duodenal mucosa in response to a meal when the intraluminal acidity increases. The synthetic version is administered by slow intravenous injection over 1 min in order to avoid side effects such as abdominal pain. The enzyme stimulates the production of pancreatic enzymes and increases the tone of the sphincter of Oddi, resulting in an increase in the caliber of the pancreatic duct. The increase in caliber can be seen by 1 min post-intravenous administration of secretin and reaches a maximum by 3–5 min, returning to normal by 5 min post-intravenous administration.

This sequence is used as an adjunct to conventional MRCP. The standard MRCP sequences are obtained followed by the dynamic images using coronal single shot turbo spin echo sequences every 30 s for 10 min postinjection. Although secretin MRCP is not used in diagnosis or staging of pancreatic adenocarcinoma, the transient increase in pancreatic duct diameter (usually by 1 mm or more) improves the depiction of the ductal anatomy and allows differentiation of a side branch IPMN from a mucinous tumor with a high degree of accuracy [14]. This will be discussed later on in the chapter.

This sequence can also be useful in the assessment of patency of the postoperative pancreaticoenteric ductal anastomosis.

Advantages and Disadvantages of MRI

MRI does not employ the use of ionizing radiation as in other imaging modalities, which allows investigation to be performed with no known biological harm to the patient. This is useful for pregnant patients and for patients who have multiple interval scans of the pancreas.

The main disadvantage of MRI is the length of the examination and the requirement for patients to take multiple breath-holds in order to obtain high-resolution diagnostic images.

The length of a typical MRI examination of the pancreas is around 30 min which can be a limiting factor for patients who are claustrophobic, in pain, or acutely unwell. Movement or breathing during the acquisition of the sequences can result in significant degradation of imaging quality, thus reducing the diagnostic accuracy of the investigation.

Fast sequences can be utilized for patients who are unable to hold their breath, but to the detriment of diagnostic quality.

MRI Safety

MRI is particularly useful in imaging patients where administration of nonionic iodinated CT contrast media is contraindicated such as patients with a known allergy to CT contrast. The incidence of acute adverse severe reactions associated with MR gadolinium-based contrast agents varies between 0.17% and 2.4% [15]. This is significantly lower than the rate of adverse effects associated with nonionic iodinated contrast media [16, 17] and should be considered if the patient has an allergy to CT contrast. However, studies have shown that a previous reaction to CT contrast media does increase the risk for hypersensitivity reactions to gadolinium [18].

Risk factors for immediate hypersensitivity reactions to gadolinium contrast are noted in female patients, patients with underlying allergic diseases, multiple exposures, and those with a previous hypersensitivity to MR contrast media [19]. Patients with previous hypersensitivity to gadolinium are about eight times more likely to experience a reaction which can be of a greater severity than the initial contrast reaction [20].

Corticosteroid treatment has been used a premedication to reduce the incidence and severity of hypersensitivity reactions and is effective in preventing mild reactions [21]. However, patients who have had severe reactions are still at an increased risk despite premedication [22].

The administration of limited duration corticosteroids itself poses a risk particularly in patients with infection, diabetes, and hypertension.

Nephrogenic Systemic Fibrosis

In patients with renal failure, imaging with MRI and gadolinium contrast was previously considered to be a safe alternative to nonionic CT contrast media.

However, over the last decade, a condition called nephrogenic systemic fibrosis (NSF) has come to light. NSF is a fibrotic condition caused by the deposition of gadolinium within tissues of patients with end-stage renal failure [23].

The stability of the gadolinium chelate is directly linked with the development NSF. Plasma elimination of gadolinium from the body is approximately 2 h in patients with preserved renal function. However, in patients with renal failure, plasma elimination is lengthened. This increases the risk of displacement of the gadolinium ion from its chelating ligand and the formation of gadolinium-phosphate complexes which precipitate in tissues resulting in a fibrotic response [24, 25]. The exact parameter leading to lack of stability of the gadolinium chelate is not definitively known, with a lack of consensus in the literature [26].

Due to the accumulation of fibrosis in skin and visceral tissues, skin thickening, particularly involving the extremities, is noted with the development of joint contractures and loss of mobility [27]. Fibrosis involving the liver, lungs, muscle, and heart has also been recognized [28]. In some patients, this disease can be aggressive, leading to severe disability or death.

NSF has been seen in patients with chronic renal failure with an eGFR less than 30 mL/min, resulting in an incidence of NSF in 3–5% in these patients [29, 30]. Patients with hyperphosphatemia, acidosis, or pro-inflammatory states are also at increased risk [31].

Recommendations have been published by the European Society of Uroradiology (ESUR), American College of Radiology (ACR), and Food and Drug Administration (FDA) on the use of gadolinium contrast. Some gadolinium agents are contraindicated in patients with acute and chronic renal failure (CKD 4–5) as they have the highest association with NSF: gadopentate (Magnevist), gadodiamide (Ominiscan), and gadoversetamide (optiMARK). The other gadolinium agents are recommended to be used in caution in patient with low eGFR (<30 mL/min), and multiple administration of gadolinium to be avoided within a 7-day period.

Other recommendations vary between ESUR and ACR on the use of other gadolinium agents, and the timing of dialysis post-gadolinium administration [32].

Current guidelines for patients undergoing MRI with contrast include assessment of the eGFR in patients over 60 years, a history of renal disease, hypertension, or diabetes.

Referral to these guidelines online is suggested for the most up-to-date information in the relevant country of residence.

Diagnosis and Staging of Pancreatic Adenocarcinoma

Tumor Diagnosis

On T1 weighted sequences, pancreatic adenocarcinoma is demonstrated as an ill-defined hypointense mass within the high T1 signal pancreatic parenchyma. Thus, small lesions beyond the resolution of CT or iso-attenuating lesions on CT are better defined on this sequence [33]. This is potentially useful when EUS is not available or cannot be performed.

Tumor infiltration into the peri-pancreatic tissue is depicted as a low signal mass among the high signal fat on the nonfat saturated T1 weighted sequence. This is usually depicted as nodular infiltration into the fat or along the peri-pancreatic vessels, or vascular encasement.

On the T2 weighted sequences, pancreatic adenocarcinoma is isointense to mildly hyperintense compared to background pancreas due to its fibrotic nature. This makes identification of the lesion within the pancreatic parenchyma difficult. The presence of necrosis or cystic degeneration may help visualization as this will return a high signal compared to background pancreas. Assessment of the dilated pancreatic duct and its transition point is an important secondary sign of the presence of a mass lesion, and is well visualized on this sequence and on MRCP.

Administration of intravenous gadolinium contrast increases the conspicuity of tumors and improves the detection rate of small tumors (less than 2 cm) [34, 35].

After administration of intravenous gadolinium contrast, pancreatic adenocarcinoma demonstrates decreased enhancement compared to the pancreas on the pancreatic parenchymal phase image (35 s), with mild progressive enhancement into the delayed sequences. This is due to the desmoplastic nature of the lesion [36]. However, the tumor remains lower signal than the surrounding enhancing pancreas. This is differentiated from inflammatory lesions which demonstrate increased enhancement compared to the pancreas on the delayed contrast enhanced scans.

Diffusion sequences have been shown to be useful in the identification of the pancreatic adenocarcinoma from background pancreas by visual assessment on the DW images and by quantification on the ADC map [37,38,39,40]. Pancreatic adenocarcinoma is bright on the high “b” value DW images compared to the background pancreas and returns a lower ADC value on quantitative analysis.

Small pancreatic tumors have been shown to demonstrate restricted diffusion, as shown in cases of neuroendocrine tumors [41].

In patients with chronic pancreatitis, identification of adenocarcinoma may not be reliable. The inherent high signal of the pancreas on the T1 weighted sequence is lost in both pathologies, making differentiation on this sequence difficult. Chronic pancreatitis may also appear hyperintense on the high b value DW images making visual assessment on this sequence misleading [42]. However, ADC values have been shown to differ with adenocarcinoma returning a lower ADC value than chronic pancreatitis, and can be useful if there is a high index of suspicion of adenocarcinoma within chronic pancreatitis.

Although diffusion weighted imaging may be useful in differentiating benign from malignant mass lesions [37, 38], to date, there are only a few studies looking at characterization of different solid pancreatic lesions using DWI. Studies have shown there is a wide overlap in ADC quantification in differing solid pancreatic lesions making accurate characterization difficult [40, 43]. Studies have also looked DWI of adenocarcinoma with different histopathological grades, but the findings are still unclear if DWI can be helpful here [8].

Occasionally the primary malignancy can be difficult to appreciate on imaging. The secondary signs of pancreatic adenocarcinoma include pancreatic duct dilatation, atrophy of the pancreas distal to the tumor, and dilated collateral vessels due to venous invasion of the tumor. These signs can be the only indication of the presence of a mass (Fig. 1).

Fig. 1
figure 1

CT and MR findings of a pancreatic adenocarcinoma in the neck of pancreas. (a) Axial contrast enhanced CT demonstrating a nonspecific hypo/ iso-dense swelling of the head of pancreas with no defined mass (white arrow). (b) Axial T1w noncontrast image demonstrating a hypointense mass (white arrow) within the pancreas. (c) Post-contrast coronal T1w fat saturated image demonstrating a hypoenhancing mass with a normally enhancing pancreatic head. (d) Diffusion weighted images at a high “b” value demonstrating restricted diffusion (white arrow) (Images courtesy of Dr. R Albazaz, Leeds Teaching Hospital NHS trust)

Vascular Resectability

The extent of vascular involvement by pancreatic adenocarcinoma is best depicted on post-contrast multidetector CT imaging with 3-D reformats. Gadolinium-enhanced MRI is inferior to multidetector CT in terms of spatial resolution and 1.5 T MRI does not provide isotropic imaging in order to obtain 3-D reformatting.

However, with the advent of 3.0 T MRI scanners, 3-D gradient echo images have become available enabling reconstructions of 1–1.5 mm slice thickness in order to obtain accurate vascular assessment. Here, MRI with MR angiography has shown to have similar sensitivities of determining resectability compared to multidetector CT (approximately 90%) [44]. Assessment for vascular staging is the same for CT staging and is described in the chapter “Pancreatic Adenocarcinoma: CT and PET/CT” (Fig. 2).

Fig. 2
figure 2

MR images demonstrating an uncinate process mass with vascular compromise. (a) Axial T1 in-phase scan demonstrating the low signal uncinate process mass (black arrow) with rim of normal high T1 signal pancreas (white arrow). (b) MRCP sequence demonstrating a dilated pancreatic duct with sharp cutoff at the uncinated process of pancreas (white arrow). (c) Axial T1 fat saturated post-contrast arterial phase scan demonstrating the hypoenhancing uncinate process tumor with encasement of the superior mesenteric artery. (d) Axial T1 fat saturated post-contrast portal venous phase scan demonstrating the hypoenhancing uncinate process tumor with involvement of the posterior wall of the superior mesenteric vein (white arrow)

Assessment for Enucleation of Pancreatic Lesions

Enucleation surgery has been performed for small cystic tumors, neuroendocrine lesions, and IPMN.

MRI is particularly useful in the surgical assessment of the lesions. The combination of the T1 and T2 weighted images allows accurate assessment of the distance of the pancreatic lesion from the pancreatic duct to avoid involvement of the duct during surgery.

Nodal Disease

Accurate nodal staging has been shown not to be reliable on cross-sectional imaging. Where size criteria were historically used to differentiate benign from malignant nodes, this has shown not to be accurate [45] with presence of micro-metastases occurring in normal appearing lymph nodes. Nodes are more difficult to see on MRI sequences than CT, but the presence of necrosis within a node does significantly increase the suspicion of malignant infiltration.

Liver Metastases

MRI is able to detect liver lesions with a high degree of sensitivity (81–92%) compared to multidetector CT (70–87%) [46]. The addition of diffusion weighted sequences has led to the ability to detect very tiny liver lesions not seen on other modalities or on other MR sequences [47, 48].

Characterization and detection of liver lesions is significantly increased with the use of hepatocyte specific contrast agents (gadoxetate disodium, Primovist, Bayer, Germany or gadobenate dimeglumine, MultiHance, Bracco, Princeton, NJ). This type of contrast agent is taken up by the hepatocytes and is excreted via hepatobiliary system.

The enhancement of liver on the dynamic contrast arterial, portal venous, 1 and 5 min delayed phase scans is similar to the other extracellular gadolinium contrast agents. Specific liver uptake of the contrast by hepatocytes results in optimal contrast enhancement of the liver on the delayed phase scans (20–40 min for gadoxetate disodium, and 60 min for gadobenate dimeglumine). Smaller liver lesions are clearly delineated against the uniformly enhancing background pancreas. Due to the excretion of contrast by the hepatobiliary system, the biliary tract is also well visualized on the delayed scans.

Liver metastasis secondary to pancreatic adenocarcinoma tends to be hypovascular. The lesions are hypointense on T1 weighted sequences, iso- to moderately hyperintense on T2 weighted sequences, and can have a target appearance. They demonstrate irregular rim enhancement post-contrast (Fig. 3).

Fig. 3
figure 3

Selected images demonstrating liver metastases secondary to pancreatic adenocarcinoma. (a) Axial T2 weighted images of the liver demonstrating several liver metastases with a target-like appearance. Two of the lesions have been arrowed with a white arrow. There is also ascites in the upper abdomen. (b) DWI images demonstrating restricted diffusion of these visualized two lesions on this slice (white arrow). (c) Axial T1 weighted fat saturated post-contrast scans demonstrating irregular rim enhancement of these metastases (white arrow)

Wedge-shaped perilesional transient enhancement on the arterial phase is seen typically with pancreatic adenocarcinoma metastases, and not seen in neuroendocrine liver metastases. Pancreatic adenocarcinoma liver metastases in the periphery of the liver tend to be hypervascular and maybe only seen transiently on the arterial phase scan [49].

Tumor Assessment Post-neo-Adjuvant Chemotherapy

Patients with borderline resectable disease who have been treated with chemotherapy to downstage the tumor have repeat imaging prior to surgical consideration. In both CT and MRI imaging, the posttreatment fibrosis results in over-staging of local disease with both CT and MRI demonstrating a reduced sensitivity and specificity in predicting vascular involvement and resectability post-chemotherapy [50].

Mimics of Pancreatic Adenocarcinoma

Fatty Changes

Fatty replacement within the pancreas is usually diffuse, but not so rarely, can be focal and typically present in the anterior aspect of the pancreatic head. This can mimic a mass on CT or ultrasound. Due to the availability of fat and nonfat suppressed sequences, MRI is of choice for definitive diagnosis.

On the T1 weighted sequence, the fatty lesion is typically iso- or hyperintense to the pancreas. On the T1 fat saturated sequences, the area of fat will suppress appearing low signal compared to the remainder of the pancreas [51]. Post-contrast, there is homogenous enhancement of the pancreas, thus differentiating focal fatty change from adenocarcinoma.

Mass-Forming Pancreatitis

Focal pancreatitis and pancreatic adenocarcinoma can be difficult to differentiate on imaging and may lead to unnecessary surgical resection. In the absence of tissue confirmation by EUS FNA, MRI can be useful in differentiating the two pathologies.

Focal pancreatitis is usually more defined than pancreatic adenocarcinoma but also returns a low signal on T1 weighted sequence. As with adenocarcinoma, pancreatitis demonstrates reduced enhancement compared to the background pancreas, but demonstrates progressive enhancement on the delayed contrast images, more so than adenocarcinoma, and can enhance to a greater extent than the normal pancreatic tissue. Subtle findings also include preservation of pancreatic architecture if the inflammation is not marked, whereas this architecture is destroyed in adenocarcinoma.

However, it can be impossible to differentiate the two pathologies on imaging, and follow-up imaging in about 4–6 weeks is advised if the clinical features favor pancreatitis.

Mass-forming autoimmune pancreatitis (AIP) is another mimic of adenocarcinoma on both imaging and histology. Homogenous enhancement of mass-forming AIP on the arterial and portal venous phase sequences differentiate this from pancreatic adenocarcinoma, as well as the preserved architecture of the pancreas. The duct penetration sign, where the main pancreatic duct penetrates the mass is a specific finding in an inflammatory pancreatic mass lesion. This appearance is different to pancreatic adenocarcinoma where there is an abrupt cutoff of the pancreatic duct at the site of the mass (Fig. 4).

Fig. 4
figure 4

Selective images of a mass forming AIP pre and posttreatment. (a) Axial contrast enhanced CT scan demonstrating a slightly hypodense expanded pancreatic head (white arrow) in keeping with a mass. (b) Axial T2 weighted sequence of the head of pancreas which is slightly higher signal than muscle. (c) Coronal T2 weighted sequence demonstrating the high signal pancreatic duct penetrating the mass (white arrow). (d) MRCP sequence demonstrating the dilated pancreatic duct with a tapering and penetrating into the pancreatic head (white arrow). (e) Axial T2 weighted scan of the pancreatic head which appears normal in size with a normal pancreatic duct (white arrow), 4 weeks post-steroid treatment. (f) Axial portal venous phase scan of a normally enhancing pancreatic head (Images courtesy of Dr. R Albazaz, Leeds Teaching Hospital NHS trust)

Lower ADC values in mass-forming AIP have also been shown to be useful in differentiating the two pathologies, but this finding has not always been consistent in the literature with substantial overlap in the ADC values [52]. Other features of AIP are the halo sign, with a thin rim of fluid around the pancreas and evidence of autoimmune disease in other organs.

Other Solid Pancreatic Tumors

Solid Pseudopapillary Tumor

Solid pseudopapillary tumor of the pancreas represents 1–2% of pancreatic tumors. These are of low-grade malignant potential and predominantly occur in younger women. They are usually large (mean 9 cm), located within the tail and are well demarcated with a thick solid capsule which enhances post-contrast. On the dynamic contrast enhanced scans, there is variable enhancement ranging from a hypervascular mass with washout to slow enhancement on the arterial phase with progressive enhancement to into the delayed phase [53]. The mass tends to displace surrounding structures rather than invading them. Due to hemorrhage, the lesion can exhibit solid and cystic components, and as a consequence demonstrate high signal on the T1w sequence and appear cystic on the T2w sequence, differentiating this from pancreatic adenocarcinoma [54].

Pancreatic Neuroendocrine Tumors (NET)

Functioning NET are identified primarily from symptoms due to the secretion of hormones rather than identification of a mass on imaging. These lesions tend to be small at diagnosis (less than 3 cm) and can be elusive on cross-sectional imaging.

These lesions are well defined, low signal on the T1 weighted sequences, but demonstrate higher signal on the T2 weighted sequences compared to the background pancreas and can appear cystic with a thickened wall. They are hypervascular demonstrating intense arterial enhancement post-contrast. They can also demonstrate ring enhancement. Malignant endocrine neoplasms tend to demonstrate restricted diffusion, but the ADC values do to vary due to tumor differentiation, hemorrhage, and necrosis [55] (Fig. 5).

Fig. 5
figure 5

Selected images of a NET of the posterior body of pancreas with cystic degeneration. (a) Axial T1 fat saturated images demonstrating the low signal lesion within the high signal pancreas (white arrow). (b) Axial T2 image demonstrates the lesion returning a high signal. (c) DWI images with restricted diffusion of the rim of the lesion (white arrow). (d) ADC map with low signal rim in keeping with restricted diffusion (white arrow). (e) Axial post-contrast portal venous image demonstrating rim enhancement of the NET (white arrow) (Images courtesy of Dr. R Albazaz, Leeds Teaching Hospital NHS trust)

Nonfunctional endocrine tumors tend to be much larger in size at presentation due to the lack of hormone secretion and symptoms. These lesions exhibit calcification, cystic/necrotic degeneration, and vascular invasion. The vascular invasion tends to be fingerlike intravascular solid tumor thrombus within the affected vessels, a feature not usually seen in patients with adenocarcinoma. Enhancement is varied due to the necrosis and calcification, but the solid areas are typically hypervascular [56, 57].

Lymphoma

Primary pancreatic lymphoma is rare and seen usually in immunocompromised patients. This is commonly the B cell type of non-Hodgkin’s lymphoma and can either be a focal well-circumscribed lesion or a diffuse infiltration of the pancreas.

The focal type of lymphoma typically localizes at the pancreatic head with no significant dilatation of the main pancreatic duct. There can be encasement of the vessels but vascular distortion is not seen.

The diffuse form of pancreatic lymphoma can mimic acute pancreatitis.

The imaging characteristics are nonspecific, demonstrating low signal on T1 and intermediate signal on T2 weighted images, and demonstrating faint contrast enhancement [58].

Metastases to the Pancreas

Metastasis to the pancreas is relatively rare. Renal cell carcinoma metastases have a predilection for the pancreas (30%). Other malignancies include bronchogenic carcinoma (23%), breast, and colon. Renal cell carcinoma metastases are hypervascular on the arterial phase. Otherwise, metastases have variable heterogeneous enhancement and can be difficult to differentiate from adenocarcinoma [59]. However, the patient will have a history of current or previous malignancy, and the lesions may be multiple, which is not typically seen in adenocarcinoma.

Cystic Lesions of the Pancreas

The majority of cystic lesions within the pancreas are discovered incidentally on imaging, either ultrasound, CT or MRI. The incidence of these cysts is increasing, and may be in part due to the availability of high-end ultrasound, CT, and MRI scanners, and a general increase in diagnostic imaging of the population. Only rarely, are these pancreatic cystic abnormalities malignant mucinous lesions.

Serous Cystic Lesions

Serous cyst adenoma of the pancreas is considered to be a benign entity, seen in older female patients with only very rare cases of malignant degeneration.

These lesions typically contain multiple tiny cysts (less than 2 cm) with a central stellate calcified scar giving a honeycomb appearance. On CT, these can look solid and can mimic pancreatic adenocarcinoma. On MRI, the multiple cysts are clearly delineated on the T2w sequences where fluid is bright, with the low signal delayed enhancing central scar enabling a confident diagnosis. There is no dilatation of the pancreatic duct and no pancreatic atrophy (Fig. 6).

Fig. 6
figure 6

Selected images demonstrating a serous cystic lesion in the tail of pancreas. (a) Axial T2 weighted image demonstrating a mass with several small cysts and a central low signal scar (white arrow). (b) Axial T2 weighted image demonstrating a normal caliber distal pancreatic duct (white arrow) and no pancreatic atrophy

Mucinous Tumors of the Pancreas

Mucinous cystic neoplasms occur more often in women, seen within the body or tail of the pancreas, and have a higher malignant potential. These lesions have a range of histology. The most recent WHO update classifies lesions from benign mucinous lesions with low to intermediate grade dysplasia (previously termed cystadenoma), to mucinous lesions with high grade dysplasia (previously termed cystadenocarcinoma), and mucinous tumors with associated invasive carcinoma.

Mucinous cysts are larger than other neoplastic cysts, lobulated and exophytic and are typically unilocular with a few septations. The lesions have thick enhancing walls with septations, calcifications, and occasionally solid papillary excretions. Again, these are usually high signal on the T2 sequences but given their mucin component, can demonstrate variability in signal characteristics, including high signal on T1 weighted images.

These are differentiated from side branch intraductal papillary mucinous neoplasms (IPMN) by lack of connection to the main pancreatic duct on the MRCP sequences [60].

Increased risk factors for adenocarcinoma or high-grade dysplasia in mucinous cystic neoplasms are the male sex, pancreatic head and neck location, larger lesions, solid components or mural nodules, and pancreatic duct dilatation [61].

Intraductal Papillary Mucinous Neoplasms (IPMN)

IPMN arise from the main pancreatic duct or the side branches. Three types of IPMN are recognized: the side-branch IPMN, main branch IPMN, and mixed type IPMN.

MRCP imaging is the most useful noninvasive imaging modality to assess for IPMN. The pancreatic duct and side branches are well delineated on the T2 weighted sequences and MRCP sequences.

Side branch IPMN are most commonly identified in the uncinate process of the pancreas and appear septated or lobulated. However, they can be found elsewhere within the pancreas and can appear as unilocular cystic foci. Although more commonly solitary, they can be multifocal in 40% of cases.

The presence of a side-branch IPMN can be reliably depicted where communication between a cystic lesion and the main pancreatic duct is shown. However, this may not be reliably identified on imaging.

Studies have shown a low risk of malignancy if there are no solid components, no dilatation of the main pancreatic duct and the cysts measure less than 3 cm [62, 63].

Worrisome features of a cystic lesion in the pancreas include a cyst of greater than 3 cm, thickened enhancing cyst wall, abrupt change in the caliber of the main pancreatic duct with distal pancreatic atrophy, nonenhanced mural nodules, and lymphadenopathy. Cysts with high risk stigmata are lesions with an enhancing solid component and a main pancreatic duct greater than 10 mm [64] (Fig. 7).

Fig. 7
figure 7

Selected images of a pancreatic cyst in the tail of pancreas with a mural nodule. (a) Axial T1 sequence demonstrating a low signal lesion in the tail of pancreas (white arrow). (b) Axial T2 sequence demonstrating the cyst with a mural nodule (white arrow). (c) MRCP sequences demonstrating the cyst with internal mural nodule, and good overview of the pancreatic and biliary ductal system. (d) Axial contrast enhanced scan in portal venous phase demonstrating thick rim enhancement and mild enhancement of the mural nodule

Main branch IPMN carries a higher risk of malignancy of between 23% and 57% [65] and management is often surgical. Features include dilatation of the main pancreatic duct of more than 5 mm, either diffuse or segmental dilatation in the absence of an obstructive lesion. The side branches can be dilated, and small mural nodules can be identified. The pancreatic parenchyma becomes atrophied, particularly with increasing ductal dilatation.

The main branch IPMN type is clearly depicted on the MRCP and T2 weighted sequences and accurate measurements can be performed to demonstrate the extent and caliber of dilatation and stricturing of the pancreatic duct.

The excellent soft tissue contrast between high signal fluid and low signal soft tissue on the T2 weighted sequences of MRCP enables accurate detection of solid papillary projections and mass formation within an IPMN undergoing malignant transformation.

The presence of a solid mass, dilatation of the main pancreatic duct to over 10 mm diameter, diffuse or multifocal involvement, and calcified intraluminal content are specific signs of malignancy [66].

MRI is the preferred imaging modality for the follow-up and management of IPMN due to the superior delineation of these lesions on the T2 weighted and post-contrast sequences. The lack of ionizing radiation allows for repeated interval imaging without risk of radiation burden to the patient [67, 68]. The management of cystic neoplasms is discussed in chapter “Management of Cystic Neoplasms of the Pancreas Including IPMNs”.

Conclusion

With recent advances in the technology of magnetic resonance imaging, MRI is being increasingly utilized in the imaging of pancreatic lesions. It is a particularly useful problem-solving tool in the evaluation of pancreatic cysts, identification of small pancreatic lesions beyond the resolution of CT, and has increasingly potential use in differentiating benign from malignant pancreatic lesions. The ability to clearly visualize the pancreatic duct and define this from a pancreatic lesion makes MRI invaluable in the preoperative assessment prior to enucleation surgery.

For staging, with the advent of 3 T MRI, the ability of vascular staging is becoming comparable to CT. MRI with diffusion weighted imaging and gadolinium contrast has been shown to be far superior to CT in the detection of liver metastases, and its use prior to consideration of pancreatic surgery may have a significant impact on patient outcome.

However, MRI is not without its risk, particularly for contrast enhanced scans. Patients with known relevant risk factors must be assessed prior to consideration of contrast enhanced MRI and the consequences may be severe.

Cross-References