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Imaging in pancreas transplantation
C H A P T E R
16 Imaging in pancreas transplantation Brenda Lee Holbert, Neeraj Lalwani Wake Forest School of Medicine, Department of Radiology, Wake Forest Baptist Medical Center, Winston-Salem, North Carolina, United States O U T L I N E Preoperative planning: Imaging of potential recipient 195 Preoperative planning: Imaging of donor
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Preoperative planning: Imaging of potential recipient Potential pancreas transplant recipients undergo imaging to uncover any impediments to the planned placement and anastomoses of the transplant and to screen for diseases that may place the patient at high risk. The patients are diabetics, so vascular disease is expected. The extent of aortoiliac calcification is assessed to guide transplant placement. Screening for occult mass or neoplasm is important because the posttransplantation immunosuppression regimen can speed tumor progression. Typically, a chest radiograph and an unenhanced computed tomography (CT) of the abdomen and pelvis constitute the preoperative workup. Occasionally the findings lead to additional imaging.
Preoperative planning: Imaging of donor Whole organ transplantation can be done from a deceased donor. Depending on the cause of the donor’s death, various imaging may be available. If CT images
Transplantation, Bioengineering, and Regeneration of the Endocrine Pancreas, Volume 1 https://doi.org/10.1016/B978-0-12-814833-4.00016-2
Complications Vascular complications Nonvascular complications Bowel complications Posttransplant lymphoid proliferative disorders
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are available, donor anatomic variants and suitability of organs for donation can be assessed prior to organ procurement (Fig. 1). In most cases, multiple abdominal organs from a single donor are distributed to several recipients. The procurement team must separate the organs while maintaining viability, with the preservation of the major blood vessels for each donor organ to enable anastomosis into the recipient. The pancreas and liver share blood supply and drainage. Blood vessels, such as the portal vein, celiac axis branches, and sometimes replaced right hepatic artery from the superior mesenteric artery (SMA), must be divided properly so that both organs remain perfused. The celiac axis and its hepatic artery branches remain with the liver. The splenic artery, which is a branch of the celiac axis, is harvested to remain with the donor pancreas as the splenic artery supplies the pancreatic body and tail. The donor SMA is harvested to supply the donor pancreas head via its branch, the inferior pancreaticoduodenal artery (IPDA). In donors with typical anatomy, a celiac axis branch, the gastroduodenal artery (GDA), must be ligated during organ harvest. The GDA branch to the pancreas is the superior pancreaticoduodenal
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a rtery which supplies the head of the pancreas. In the donor pancreas, this part of the pancreatic head is supplied by collateral flow from the IPDA. Since the SMA gives rise to the IPDA, and the splenic artery is a branch of the celiac artery, the harvested donor pancreas has two separate arterial stumps. Usually, a Y-graft is formed from donor iliac arteries to make a common conduit for arterial blood supply the donor pancreas. Donor pancreas venous drainage is by intrapancreatic tributaries into the splenic and superior mesenteric veins (SMVs), which coalesce into the portal vein. Generally, 1–2 cm of the donor portal vein is harvested with the donor pancreas. In most cases, the majority of the donor portal vein stays with the donor liver. In order for the pancreas allograft to function, the pancreas duct must drain its digestive juices into the recipient. Rather than ligation of the duct at donor harvest, the current procurement practice is to keep the donor ductal system intact by including the segment of duodenal C-loop into which the pancreatic duct drains as part of the harvested tissue.
know the configuration of the anastomoses so that the appropriate structures are imaged (Fig. 2). The arterial anastomosis for the pancreas allograft is usually at recipient common iliac artery or external iliac artery to the transplant Y-graft conduit. The blood flows into the two limbs of the conduit. One limb supplies the pancreatic head via SMA to IPDA. The other limb supplies the pancreatic body and tail via the splenic artery. The Y-graft length is tailored for patient anatomy and may be long if the graft is placed in mid-abdomen or short if graft is placed in the lower abdomen. The donor portal vein is the conduit for the venous drainage to a recipient vein. The donor portal vein may be anastomosed to the recipient iliac vein (Fig. 2A) or the recipient IVC or the recipient SMV. In cases where the donor portal vein drains to the recipient SMV (Fig. 2B), the blood flows into the recipient’s portal system. In cases where the donor portal vein drains into the recipient’s iliac vein or IVC, the blood drains into the donor’s systemic veins. Venous drainage of a native pancreas is into the portal system, which allows the liver to metabolize the pancreatic hormones. Therefore, venous drainage of a transplant pancreas via the recipient portal system emulates native pancreas physiology and intuitively should allow better function. However, either portal or systemic venous drainage yields similar clinical results thus far.1–3 Both methods are still used. For exocrine drainage, usually the donor duodenal C-loop is anastomosed to the recipient small intestine. Various approaches can be successful. Some surgeons prefer a side-to-side anastomosis; others prefer Rouxen-Y. The pancreatic head may face cranially and be in the abdomen rather than in the anatomic pelvis. Historically, the common surgical solution for exocrine drainage was donor duodenal C-loop anastomosis to the urinary bladder with the pancreatic head oriented caudally in the recipient anatomic pelvis and tail positioned more cranially (Fig. 2C). With this surgery, the pancreatic duct drains into the urinary bladder lumen, and pancreatic excretions mix with urine. Pancreatic function can be checked with urinalysis. This approach is still used at some institutions and for some patients, especially in those who do not have a simultaneous renal transplant,3 but complications, such as chemical cystitis, urethritis, and, for males, urethral leak and stricture, are serious drawbacks.4–6 Some patients have successfully undergone surgical revision to convert from exocrine drainage via urinary bladder to exocrine drainage via bowel4, 7 (Fig. 3).
Postoperative imaging
Sonography
Multiple surgical techniques have been devised for pancreatic transplantation. To image the pancreas transplant, the technologist needs to know the location of the pancreas allograft within the recipient and may need to
Sonography is the primary imaging tool for pancreatic transplant assessment. This modality is noninvasive, uses no ionizing radiation, and can be done at the patient’s bedside. Patient body habitus, depth of
FIG. 1 Donor pancreas. The arterial supply to the tail and body is from the splenic artery (SA). The arterial supply to the head is from the inferior pancreaticoduodenal (IPDA) artery, a branch of the superior mesenteric artery (SMA). The SA and SMA stumps receive flow through a Y-graft, usually constructed from donor iliac arteries. The venous drainage from the pancreas flows into the portal vein. The donor pancreas head remains attached to a short segment of donor duodenum, into which the donor pancreatic duct (not illustrated) maintains its normal drainage.
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FIG. 2 Typical pancreas transplant anatomy. (A) Posttransplant anatomy. Transplant pancreas receives its arterial supply via Y-graft from recipient common iliac artery and drains via donor portal vein into recipient common iliac vein. The transplant pancreatic head and duodenal segment remain intact, allowing drainage of pancreatic duct. The duodenal segment is anastomosed to recipient bowel for enteric drainage. (B) Posttransplant anatomy. Transplant pancreas receives its arterial supply via Y-graft from recipient common iliac artery and drains via donor portal vein into recipient superior mesenteric vein. The transplant pancreatic head and duodenal segment remain intact, allowing drainage of pancreatic duct. The duodenal segment is anastomosed to recipient bowel for enteric drainage. (C) Posttransplant anatomy. Transplant pancreas receives its arterial supply via Y-graft from recipient common iliac artery and drains via donor portal vein into recipient common iliac vein. The transplant pancreatic head and duodenal segment remain intact, allowing drainage of pancreatic duct. The duodenal segment is anastomosed to recipient urinary bladder and the pancreatic exocrine drainage is into the urine.
the transplanted pancreas within the patient, and configuration of bowel adjacent to the pancreas determine how complete an examination is possible. Bandages and bowel gas limit visibility of the transplant, even in the hands of very skilled sonographers. Prior to obtaining images, the ultrasound technologist either reads the operative report or checks with the transplant surgeon to confirm location of the organ and to check the configuration of the vascular and enteric anastomoses. The American College of Radiology, the American Institute of Ultrasound in Medicine, the Society for Pediatric Radiology, and the Society of Radiologists in
Ultrasound have agreed upon the following indications for ultrasound examination of the transplanted pancreas8: 1. Performance of a screening ultrasound examination to establish a baseline after transplantation as per the hospital surveillance protocol; 2. Follow-up of abnormal findings on a prior transplant ultrasound examination; 3. Assessment of graft dysfunction in patients with abnormal laboratory values or clinical parameters (such as elevated blood glucose); 4. Evaluation for suspected stenosis or thrombosis of the vasculature;
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FIG. 3 Normal transplant sonogram. (A) Grayscale sonogram image shows the normal transplant pancreas (marked by calipers) with adjacent bowel and with vessels posterior to transplant. (B, C) Color Doppler and spectral Doppler of the Y-graft conduit. Note: The color scale is set so that red indicates flow toward transducer and blue indicates flow away. In (B), the transplant pancreas is outlined by a yellow dotted line and the Y-graft conduit is marked by a long yellow arrow. In (C), the spectral waveform shows a normal rapid upstroke in systole and remains above the horizontal line in diastole, indicating flow toward the transplant pancreas. (D) Color Doppler of the transplant pancreas splenic artery supplying body and tail. In the complete study, the technologist obtains a similar image of the transplant superior mesenteric artery in the pancreatic head. Also, arterial spectral waveforms are obtained at the head, the body, and the tail. (E, F) Color and spectral Doppler of the venous outflow of transplant splenic vein and transplant portal vein. The venous waveform exhibits nearly the same velocity in systole and diastole.
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5. Evaluation of pain at or near the surgical site; 6. Evaluation of the response to treatment (such as immunosuppressive therapy in the setting of rejection); 7. Evaluation for iatrogenic injury or complications after biopsy of a transplanted pancreas; and 8. Assessment of the transplant in the setting of infection or pancreatitis. The examination consists of grayscale, color Doppler, and spectral Doppler assessment. For the grayscale assessment the technologist attempts to image the entire allograft pancreas in transverse and longitudinal planes so that its size and echogenicity can be evaluated. Grayscale images are helpful for the evaluation of pancreatic duct diameter/dilatation. Once the position and orientation of the organ are defined and parenchymal images are obtained, grayscale images of the arterial Y-graft, pancreatic arterial vasculature, and donor portal vein are obtained for the evaluation of intraluminal abnormalities. The space surrounding the transplant is assessed, and if any fluid collections are visible, the technologist obtains images. For patients with enteric drainage of the pancreatic duct (the majority of US patients), imaging of any adjacent fluid-filled bowel for dilatation is performed. For patients with urinary bladder drainage of the transplant pancreatic duct, transverse and longitudinal bladder imaging is performed. If a pancreatic stent is present, the technologist attempts visualization of proximal and distal ends. The vessels assessed by Doppler are: (1) both limbs of the transplant arterial Y-graft, (2) the transplant SMA, (3) the transplant splenic artery, (4) the recipient artery (usually the common or external iliac artery), (5) the transplant SMV, (6) the transplant splenic vein, (7) the transplant portal vein, and (8) the recipient vein (usually an iliac vein or the SMV). The arterial and venous anastomoses are assessed. Vessels are assessed with color Doppler and spectral Doppler. If necessary, power Doppler is used. Color or power Doppler images of the entire pancreas transplant are obtained to assess the global vascularity of the graft. Color Doppler allows velocities to be imaged within a fairly large region of interest for the identification of presence and direction of flow. Usually, the sonographer sets the image parameters so red indicates flow toward the transducer and blue indicates flow away from the transducer. If flow velocity is too high for the settings, an artifact called aliasing, a mixture of multiple colors, appears. If color Doppler is not technically possible, such as with very low flow, power Doppler is utilized. Power Doppler detects lower velocity flow but does not show flow direction. Spectral Doppler allows a quantitative assessment of flow, represented as a waveform. The shape and size of the waveform contain information indicating velocity and direction of blood flow over a time period.
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Samples are typically obtained for several cardiac cycles. Spectral Doppler images are obtained in the following areas: (1) within the recipient artery proximal to the Y-graft anastomosis, (2) within the Y-graft itself, (3) within the transplanted pancreas splenic artery, (4) within the transplant SMA, and (5) at any areas of color flow aliasing. Doppler indices obtained at these locations include the peak systolic velocity (PSV), and may include resistive indices (RIs). The transplant veins are assessed as well. Color and spectral Doppler images of the graft splenic vein, SMV, and portal vein to the recipient venous anastomosis are obtained. Spectral Doppler assessment of the peak velocity may be performed within the graft portal vein, at the graft portal vein-recipient venous anastomosis, and distal to the anastomosis within the recipient vein. Additional measurements at areas of color flow aliasing may be helpful. Images to demonstrate venous flow in the head and tail of the transplanted pancreas are obtained. Two additional methods of ultrasound assessment of the pancreas transplant are possible but not as widely used. One is contrast-enhanced ultrasound (CEUS). With this method, contrast designed to show blood flow and perfusion is administered intravenously. The contrast is composed of biocompatible gas-filled microspheres. With contrast enhancement, the transplant pancreas perfusion can be assessed for pattern of enhancement (homogeneous, heterogenous, or areas without enhancement), and time-intensity curves can be generated.9–12 Some research has been done regarding predictability of insulin production/function of the transplant pancreas by using the CEUS generated time-intensity curves.13 The other method is scanning with Superb Microvascular Imaging technology, which can detect very slow flow with a unique algorithm designed to differentiate motion artifact or clutter from flow.14 This technique is different from power Doppler which uses a wall filter to help detect low flow.
Computed tomography and magnetic resonance imaging These modalities may be used to supplement sonography in order to more fully characterize a finding or to solve a problem when the sonogram does not show the reason for the patient’s clinical problem. With unenhanced CT (meaning no intravenous contrast), the position and size of the transplant, peri- transplant fluid collections, and bowel obstruction can be assessed. Enteric contrast is useful for bowel leak detection. With contrast-enhanced CT, the pancreas transplant enhancement pattern can be assessed, as can vascular patency. The MRI (Fig. 4) can be performed with various techniques to focus on the pancreas allograft parenchyma
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FIG. 4 MRA: (A) Contrast-enhanced delayed T2 weighted axial image reveals a diffusely enlarged swollen transplant pancreas (yellow arrows). Blood vessels appear white with this technique. (B) The processed images show patent Y-graft arterial conduit (yellow arrow) from iliac artery with intact arteries of the allograft pancreas (circled). B = bowel.
and surrounding tissue or to focus on the vasculature or on the pancreatic duct. If the patient has poor renal function and cannot tolerate intravenous contrast, unenhanced MRI shows more information about vasculature than unenhanced CT.15
Interventional imaging Pancreatic transplant biopsies are often performed with ultrasound guidance16 (Fig. 5), especially in patients who have a pancreas transplant without a kidney transplant from the same donor. Typically, if a patient has a renal transplant from the same donor, renal transplant biopsy can predict rejection of the pancreas transplant.
Ultrasound-guided pancreas transplant biopsy is part of routine care at many institutions. The pathologist needs tissue because no pathognomonic imaging studies or serum tests are available for diagnosis of graft rejection. By the time a patient develops hyperglycemia, the allograft pancreas is in later phases of rejection and the damage is usually irreversible.17 Interventional angiography is used to treat vascular complications of pancreas transplantation with options of venous thrombectomy or thrombolysis, endovascular stent grafts, and coil embolization18–20 (Fig. 9). The CT or ultrasound guidance can be helpful in drainage procedures if the patient develops fluid collections or abscess.
Complications Some complications happen early after surgery, such as anastomotic breakdown with bowel leak, hemorrhage, and infection. Other complications are more of a threat later, such as chronic rejection or posttransplantation lymphoproliferative disorders (PTLD). Length of time from surgery to clinical presentation helps determine which imaging examinations are likely to be most helpful.
Vascular complications
FIG. 5 Ultrasound guided pancreas transplant biopsy. Visualized portion of the pancreas is outlined by a yellow dotted line. The visualized portion of the biopsy needle is the oblique white line, indicated by yellow arrows.
The most common vascular complication is venous thrombosis21, 22 (Figs. 6 and 7), which occurs about twice as often as arterial thrombosis. The splenic vein stump often has a small amount of thrombus at the blind end in the transplant pancreatic tail. If this acts as a nidus and thrombus becomes more extensive, thrombus can change from an expected finding to a complication. With
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FIG. 6 Venous thrombosis, transplant failure: (A) Color Doppler image shows a swollen, heterogeneous pancreas (outlined by yellow dots) and portions of thrombosed transplant veins (outlined in green). Color does not fill the veins, and color flow is absent in the pancreatic parenchyma. (B) Power Doppler image redemonstrates the swollen, heterogeneous pancreas (outlined by yellow dots) and splenic vein (outlined in green). Only a few pixels from the power Doppler and no stream of flow are visible. (C) Doppler calipers are on splenic artery within the pancreas. Note the spectral wave form shows reversal of flow during diastole. Splenic vein (outlined in green) does not fill with color. This pancreas failed and was explanted. B = bowel, FF = free fluid.
venous obstruction the pancreas may become enlarged and edematous. On sonography, the allograft pancreas may appear hypoechogenic or heterogenous and fluid may be present around it. If the venous obstruction is due to thrombosis, the lumen of the transplant splenic vein may contain echoes. The venous Doppler signal may be absent. The arterial spectral Doppler waveform may show reversed diastolic flow, a harbinger of disaster, because it means extensive venous obstruction, with risk of transplant infarction.23 Thrombosis, arterial, venous, or combination, is called pancreatic allograft thrombosis.24 Most publications do not distinguish between arterial or venous pancreas allograft thrombosis.21, 22 Depending on severity and chronicity, thrombosis can be treated by anticoagulation, mechanical thrombectomy, or transplant pancreatectomy (also called explantation).25
Arterial thrombosis is diagnosed by absent arterial flow on color and power Doppler and absent arterial spectral waveform. Contrast-enhanced CT may be used to demonstrate extent of thrombus (Fig. 8). As noted above, if a patient cannot receive IV contrast material, unenhanced MRI is preferred over unenhanced CT. Unenhanced MRI can demonstrate increased signal on T1-weighted sequences or loss of normal flow void, permitting a diagnosis.15, 26 Contrast-enhanced CT can demonstrate the extent of venous thrombosis, which may help determine whether anticoagulation is necessary.24 Arterial pseudoaneurysm (Fig. 9) is rare, potentially life-threatening, complication20, 27 associated with intraabdominal infections before or at the time of diagnosis. The pseudoaneurysm can occur either at an anastomosis27 or in the pancreas or nearby tissues.28
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FIG. 7 Venous thrombosis, transplant survival: (A) Color Doppler image shows homogeneous pancreas (outlined by yellow dots) with thrombosed transplant splenic vein (outlined in green). Color does not fill the vein, but color flow is present within the pancreatic parenchyma. (B) Power Doppler image redemonstrates the pancreas (outlined by yellow dots) and splenic vein (outlined in green). The power Doppler shows no splenic vein flow. (C) Doppler calipers are on splenic artery within the pancreas. Note the spectral wave form shows forward flow during diastole. Splenic vein (outlined in green) does not fill with color.
An arterial pseudoaneurysm may be detected with various imaging modalities. When the “cyst” is assessed with color Doppler, a swirling “yin-yang” appearance is observed. If spectral Doppler is used to interrogate the pseudoaneurysm neck, a biphasic to-and-fro waveform is produced.29 With CT or MRI, contrast-enhanced imaging can help in characterizing a pseudoaneurysm and a larger region of the patient’s anatomy for surgical or endovascular treatment planning.28 Arterial pseudoaneurysms in the setting of pancreas allograft can be successfully treated by stent placement or surgery.20 The rare arterial pseudoaneurysm produced during a biopsy or from surgery may have an associated arteriovenous fistula.20 A procedure can also be complicated by an arteriovenous fistula without an arterial pseudoaneurysm, which may not be visible on the grayscale sonogram. When color Doppler is applied, an area of color aliasing may show at the fistula. The spectral Doppler waveform will be high-velocity, low-resistance
aveform. The arterial waveform will have increased w diastolic flow, and the venous waveform will be pulsatile. Just as with pseudoaneurysm, if an arteriovenous fistula is seen with a sonogram, a CT or an MRI is useful to show the extent and full anatomy of the complication.29 Early venous opacification and a draining vein can sometimes be demonstrated. Many small arteriovenous fistulas spontaneously resolve. Large, hemodynamically significant arteriovenous fistulas may need to be repaired.15 Arterio-enteric and arterio-urinary fistulae are rare problems, usually in grafts with chronic rejection or that no longer function.27 Patients may present with life-threatening hemorrhage.20, 27 Because any patient with clinically significant gastrointestinal hemorrhage may get an angiogram, it is critical for the angiographer to know the pancreas transplant history so that transplant angiography could be performed before mesenteric angiography. If the angiographer performs
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FIG. 8 Arterial thrombosis of Y-graft: Axial images from contrast-enhanced CT demonstrate the Y-graft (yellow arrows). (A) Proximal conduit completely fills with contrast. (B) Proximal edge of thrombus with less enhancement inside the conduit. (C) Distal end of conduit does not fill with the contrast.
the usual mesenteric angiogram, the arterio-enteric or arterio-urinary fistula could not be imaged, and the patient may continue to have hemorrhage. Either arterial or venous stenosis may be detrimental for a pancreatic transplant. These can be detected with sonography. Stenosis creates turbulent flow, which can show aliasing on color Doppler. Spectral Doppler shows increased velocity at the stricture. Note that in the immediate postoperative time period, for up to a week, perianastomotic edema may cause a temporary narrowing that resolves as the anastomosis heals, but if findings indicating stenosis do not improve or if findings indicating stenosis newly appear after the first postoperative week, CT angiography of MR angiography are performed.15 If one of these studies confirms the diagnosis, catheter angiography, and possibly therapeutic intervention, may be performed. Venous stenosis can diffuse narrowing of the transplant portal vein regardless of whether the drainage is to recipient system or portal venous system. When this happens, long-term anticoagulant therapy may be beneficial.28
Nonvascular complications Nonvascular complications include collections such as hematoma or abscess, graft-related complications of pancreatitis with pseudocyst or walled-off necrosis, and graft-related complications of rejection. Enteric complications include bowel obstruction and bowel leak. There is also a risk of tumor, such as PTLD. Postoperative hematoma A hematoma can form at the operative site after any surgery. A small hematoma that does not compress vasculature or the pancreas allograft is expected, but a large hematoma can cause problems. With ultrasound assessment, a new hematoma appears as a smoothly marginated, moderately echogenic structure without internal vascular flow. Over time, internal architecture of a hematoma becomes more complex with varying areas of fluid. Eventually, a hematoma may liquefy. On CT, the hematoma begins as a smoothly marginated, nonenhancing, hyperattenuating structure. On CT, subacute hematomas
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FIG. 9 Pancreatic graft artery pseudoaneurysm with surrounding hemorrhage: (A–D) Axial-enhanced CT images from cranial to caudal. Axial images show enlarged, heterogeneous pancreas transplant (marked by yellow arrows) that is infiltrated from hemorrhage. Blurry white areas in the pancreas are foci of hemorrhage. Major source is a large bilobed pseudoaneurysm (marked with black asterisk), arising from the transplant SA (marked by aqua arrows). Transplant SMA is marked by +. A = aorta, B = bowel, Y = Y-graft conduit. (E) Three-dimensional reconstruction. This format allows visualization of the entire contrast-enhanced vasculature at one time. In addition to the large pseudoaneurysm, areas of focal dilatation in transplant SMA and SA (marked with blue asterisk) are visible. (F, G) Angiogram with coil embolization that thrombosed the pseudoaneurysm.
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may have internal hematocrit levels, eventually becoming hypoattenuating. The appearance on MRI depends on the age of the hematoma and how much extracellular methemoglobin is present. Postoperative abscess Abscesses can occur from surgical field contamination or other predisposing problems, such as breakdown of the bowel anastomosis. They more commonly appear during the first month after surgery.15 The classic imaging appearance of an abscess is a thick-walled, complex fluid collection with internal debris or even gas. Pancreatitis All pancreas allografts have at least mild pancreatitis right after transplantation, but most often the pancreas heals without complication.30 There is a small group of patients for whom the pancreatitis is clinically important. The imaging of pancreatitis involving a transplant pancreatitis has the same features as that of a native pancreas. In early pancreatitis, the amylase and lipase are elevated, but the pancreas appears normal with imaging. Later, the pancreas becomes globular and swollen in appearance, with loss of the normal surface undulation. The sonographic appearance of acute pancreatic transplant graft rejection and pancreatitis are indistinguishable at this swollen stage.31 Biopsy can differentiate the two.17 If the pancreatitis is severe, over time the pancreas becomes heterogeneous and can become hypoechoic. Perigraft fluid is common. Regions of parenchymal flow abnormality with hyperemia adjacent to decreased flow may be apparent on color Doppler. Vascular
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c omplications of pancreatitis include splenic vein thrombosis and pseudoaneurysm. Depending on clinical circumstances, contrast- enhanced CT may be helpful for the assessment of possible pancreatitis. The CT is useful for demonstrating the location of any pancreatic duct disruption and for showing relationships between perigraft collections and bowel. The extent of gas collections are well demonstrated with CT, while ultrasound only shows diffuse “dirty” shadowing. CT enhancement patterns can show pancreatic necrosis. Rejection Rejection is classified as acute, subacute, or chronic. Historically, acute rejection was an issue. Immuno suppression therapy has decreased acute rejection, so now chronic rejection is more likely to cause graft loss than acute rejection.15, 26 Imaging findings are not specific for rejection.26 In acute rejection, the pancreas may enlarge and appear swollen.15 The transplant duodenum also appears thickened. With chronic rejection, the pancreas eventually becomes atrophic. Resistive indices are not a reliable indicator of rejection.
Bowel complications Pancreas transplant surgery involves the bowel, which imparts the risks of bowel leak and bowel obstruction. Although anastomotic leak requires immediate surgery, the leak usually does not lead to loss of the transplant pancreas.15 The best way to detect enteric leak is CT with enteric contrast (Fig. 10), but even CT without enteric contrast sometimes demonstrates signs of leak, such as gas or fluid adjacent to bowel anastomosis or new or increased pneumoperitoneum. Imaging signs of
FIG. 10 CT with enteric contrast. Patient presented with a fever, high WBC, and severe abdominal pain. (A) Coronal format demonstrates diffusely enlarged transplant pancreas (yellow arrows) and mildly thickened wall of adjacent small bowel (light blue arrows). Contrast within bowel appears bright white and any leakage into peritoneum would increase the white or brighten appearance of a fluid collection (raise the CT density). (B) Axial image of the patient’s pelvis shows free fluid that is NOT dense. This study indicates transplant pancreas pathology, not bowel leak, is the problem. B = bowel.
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bowel obstruction can be seen on a radiographic abdominal series, but CT is often better for the visualization of a transition zone from distended to decompressed caliber bowel. Adhesions and internal hernia are two potential etiologies of obstruction.30
Posttransplant lymphoid proliferative disorders Posttransplant lymphoid proliferative disorders (PTLD) are a group of related lymphatic system disorders, ranging from benign B-cell hyperplasia to lymphoma.32 These disorders are a complication of chronic immunosuppression, found less frequently in patients who have tacrolimus as part of the immunosuppression than in patients who are not on tacrolimus.33 Recipients who are Epstein-Barr virus-negative have an increased risk of developing PTLD, especially after exposure to Epstein-Barr virus.33 Symptoms of PTLD are nonspecific, such as fevers, chills, malaise, nausea, and vomiting.34 Imaging of patients with these symptoms often includes an abdominal CT scan. With PTLD of the pancreas, diffuse pancreas enlargement (more common) or a focal pancreatic mass, often in the head, may be present.34 Numerous small intraabdominal lymph nodes may be visible.34 Some patients present with involvement of other organs with no graft involvement34 (Fig. 11). Just as the symptoms, the imaging findings are nonspecific. If present, enlarged lymph nodes point toward PTLD rather than rejection or pancreatitis. Ultrasound-guided biopsy is helpful for differentiating the process present. Although only about 1% of pancreas transplant patients develop PTLD,33 the correct diagnosis is critical because treatment is the opposite of therapy for rejection. The treatment for PTLD is immune system stimulation.
FIG. 11 Metastatic PTLD. Chest radiograph of patient who became infected with EBV and CMV after her transplant. In addition to pulmonary nodules, she had liver lesions and mildly enlarged abdominal lymph nodes. The transplant pancreas was not enlarged.
Conclusion Imaging of the pancreas transplant patient is valuable for sorting out complications that have similar clinical presentations. An understanding of the particular surgical anatomy is critical for optimal imaging assessment. Sonography is used for routine evaluation of the allograft and its vasculature. If sonography is limited or if complications are only partly visualized or not well assessed with this modality, CT is beneficial for assessing complications outside the pancreatic graft itself, such as bowel obstruction or leak. If a patient cannot tolerate intravenous contrast, MR is an excellent method to visualize vasculature and duct. Interventional imaging is of assistance for this patient population, with ultrasound-guided biopsy being most common. Other procedures, such as image-guided fluid aspiration or abscess drainage and diagnostic and therapeutic angiography procedures, can improve the clinical course if the patient has a complication.
References 1. Oliver JB, Beidas A-K, Bongu A, Brown L, Shapiro ME. A comparison of long-term outcomes of portal versus systemic venous drainage in pancreatic transplantation: a systemic review and meta-analysis. Clin Transplant. 2015;29:882–892. https://doi. org/10.1111/ctr.12588. 2. Bazerbachi F, Selzner M, Marquez MA, et al. Portal venous versus systemic venous drainage of pancreas grafts: impact on long-term results. Am J Transplant. 2012;12:226–232. https://doi. org/10.1111/j.1600-6143. 2011.03756.x. 3. Rogers J, Farney AC, Orlando G, Farooq U, Al-Shraideh Y, Stratta RJ. Pancreas transplantation with portal venous drainage with an emphasis on technical aspects. Clin Transplant. 2014;28:16–26. https://doi.org/10.1111/ctr.12275. 4. Dumas MD, Bude RO, Sonda IIIPL, Cohan RH, Merion RM. Urethral disruption with urinary extravasation: a delayed complication of pancreatic transplantation. Radiology. 1996;201:761–765. https://doi.org/10.1148/radiology.201.3.8939228. 5. Sollinger HW, Odorico JS, Knechtle SJ, D’Alessandro AM, Kalayoglu M, Pirsch JD. Experience with 500 simultaneous pancreas-kidney transplants. Ann Surg. 1998;228:284–296. 9742912. PMC1191479. 6. Hickey DP, Bakthavatsalam R, Bannon CA, O’Malley K, Corr J, Little DM. Urological complications of pancreatic transplantation. J Urol. 1997;157:2042–2048. https://doi.org/10.1016/S00225347(01)64670-6. 7. Knight S, Vogel T, Friend P. Pancreas transplantation. Surgery. 2017;35(7):397–403. https://doi.org/10.1016/j.mpsur.2017.04.010. 8. ACR-AIUM-SPR-SRU practice parameter for the performance of an ultrasound examination of solid organ transplants. In: ACR Practice Parameter Solid Organ Transplants. 2014. (Resolution 25). 9. Kersting S, Ludwig S, Ehehalt F, Volk A, Bunk A. Contrast-enhanced ultrasonography in pancreas transplantation. Transplantation. 2013;95(1):209–214. https://doi.org/10.1097/TP.0b013e31827864df. 10. Rennert J, Farkas S, Georgieva M, et al. Identification of early complications following pancreas and renal transplantation using contrast enhanced ultrasound (CEUS)—first results. Clin Hemorheol Microcirc. 2014;58(2):343–352. https://doi.org/10.3233/ CH-131675.
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11. Ito T, Kenmochi T, Nishikawa T, et al. A novel screening test for detecting graft thrombosis after pancreatic transplantation using contrast-enhanced ultrasonography with sonazoid. Transplant Proc. 2014;46(6):1917–1919. https://doi.org/10.1016/j. transproceed.2014.05.071. 12. Boggi U, Morelli L, Amorese G, Bargellini I, Marchetti P, Mosca F. Contribution of contrast-enhanced ultrasonography to nonoperative management of segmental ischemia of the head of a pancreas graft. Am J Transplant. 2009;9(2):413–418. https://doi. org/10.1111/j.1600-6143.2008.02475.x. 13. Aida N, Kenmochi T, Ito T, et al. Prediction of insulin secretion ability with microcirculation evaluated by contrast-enhanced ultrasonography in pancreas transplantation. Pancreas. 2018;47(5):617–624. https://doi.org/10.1097/MPA.0000000000001051. 14. Tokodai K, Miyagi S, Nakanishi C, et al. The utility of superb microvascular imaging for monitoring low velocity venous flow following pancreas transplantation: report of a case. J Med Ultrason. 2018;45:171–174. https://doi.org/10.1007/s10396-017-0795-4. 15. O’Malley RB, Moshiri M, Osman S, Menias CO, Katz DS. Imaging of pancreas transplantation and its complications. Radiol Clin North Am. 2016;54(2):251–266. https://doi.org/10.1016/J. RCL.2015.09.012. 16. Klassen DK, Weir MR, Cangro CB, Bartlett ST, Papadimitriou JC, Drachenberg CB. Pancreas allograft biopsy: safety of percutaneous biopsy—results of a large experience. Transplantation. 2002;73(4):553–555. 1188942. 17. Yates A, Parry C, Stephens M, Eynon A. Imaging pancreas transplants. Br J Radiol. 2013;86:20130428. https://doi.org/10.1259/ bjr.20130428. 18. Stockland AH, Willingham DL, Paz-Fumagalli R, et al. Pancreas transplant venous thrombosis: role of endovascular interventions for graft salvage. Cardiovasc Intervent Radiol. 2009;32(2):279–283. 19. Han K, Ko HK, Tsauo J, et al. Endovascular management for the treatment of pancreas transplant venous thrombosis: a single- center experience. J Vasc Interv Radiol. 2016;27(6):882–888. https:// doi.org/10.1016/j.jvir.2016.02.022. 20. Yadav K, Young S, Finger EB, et al. Significant arterial complications after pancreas transplantation—a single-center experience and review of literature. Clin Transplant. 2017;31:e13070. https:// doi.org/10.1111/ctr.13070. 21. Muthusamy SR, Giangrande PL, Friend PL. Pancreas allograft thrombosis. Transplantation. 2010;90(7):705–707. https://doi. org/10.1097/TP.0b013e3181eb2ea0. 22. Burke III GW, Ciancio G, Figueiro J, et al. Hypercoagulable state associated with kidney-pancreas transplantation. Thromboelastogram directed anti-coagulation and implications
23.
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for future therapy. Clin Transplant. 2004;18:423. https://doi. org/10.1111/j.1399-0012.2004. 00183.x. Harbell JW, Morgan T, Feldstein VA, et al. Splenic vein thrombosis following pancreas transplantation: identification of factors that support conservative management. Am J Transplant. 2017;17:2955– 2962. https://doi.org/10.1111/ajt.14428. Hakeem A, Chen J, Iype S, et al. Pancreatic allograft thrombosis: suggestion for a CT grading system and management algorithm. Am J Transplant. 2018;18:163–179. https://doi.org/10.1111/ ajt.14433. Barrufet M, Burrel M, Angeles Garcia-Criado M, et al. Pancreas transplants venous graft thrombosis: endovascular thrombolysis for graft rescue. Cardiovasc Intervent Radiol. 2014;37(5):1226–1234. https://doi.org/10.1007/s00270-013-0799-4. Vandermeer FQ, Manning MA, Frazier AA, Wong-You-Cheong JJ. Imaging of whole-organ pancreas transplants. Radiographics. 2012;32:411–435. https://doi.org/10.1148/rg.322115144/-/DC1. Fridell JA, Johnson MS, Goggins WC, et al. Vascular catastrophes following pancreas transplantation: an evolution in strategy at a single center. Clin Transplant. 2012;26:164–172. https://doi. org/10.1111/j.1399-0012.2011.01560.x. Tolat PP, Foley WD, Johnson C, Hohenwalter MD, Quiroz FA. Pancreas transplant imaging: how I do it. Radiology. 2015;275: 14–27. https://doi.org/10.1148/radiol.15131585. Dillman JR, Elsayes KM, Bude RO, Platt JF, Francis IR. Imaging of pancreas transplants: postoperative findings with clinical correlation. J Comput Assist Tomogr. 2009;33(4):609–617. Sandrasegaran K, Lall C, Berry WA, Hameed T, Maglinte DD. Enteric drainage pancreatic transplantation. Abdom Imaging. 2006;31:588–595. Liong SY, Dixon RE, Chalmers N, Tavakoli A, Augustinve T, O’Shea S. Complications following pancreatic transplantations: imaging features. Abdom Imaging. 2011;3(6):206–214. https://doi. org/10.1007/s00261-010-9632-6. Petrara MR, Giunco S, Serraino D, Dolcetto R, De Rossi A. Minireview. Post-transplant lymphoproliferative disorders: from epidemiology to pathogenesis-driven treatment. Cancer Lett. 2015;369:37–44. https://doi.org/10.1016/j.canlet.2015.08.007. Jackson K, Ruppert K, Shapiro R. Post-transplant lymphoproliferative disorder after pancreas transplantation: a United Network for Organ Sharing database analysis. Clin Transplant. 2013;27: 888–894. https://doi.org/10.1111/ctr.12252. Meador TL, Krebs TL, Wong-You-Cheong J, Daly B, Keay S, Bartlett S. Imaging features of posttransplantation lymphoproliferative disorder in pancreas transplant recipients. AJR. 2000;174:121–124. https://doi.org/10.2214/ajr.174.1.1740121.
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16 Imaging in pancreas transplantation Brenda Lee Holbert, Neeraj Lalwani Wake Forest School of Medicine, Department of Radiology, Wake Forest Baptist Medical Center, Winston-Salem, North Carolina, United States O U T L I N E Preoperative planning: Imaging of potential recipient 195 Preoperative planning: Imaging of donor
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Preoperative planning: Imaging of potential recipient Potential pancreas transplant recipients undergo imaging to uncover any impediments to the planned placement and anastomoses of the transplant and to screen for diseases that may place the patient at high risk. The patients are diabetics, so vascular disease is expected. The extent of aortoiliac calcification is assessed to guide transplant placement. Screening for occult mass or neoplasm is important because the posttransplantation immunosuppression regimen can speed tumor progression. Typically, a chest radiograph and an unenhanced computed tomography (CT) of the abdomen and pelvis constitute the preoperative workup. Occasionally the findings lead to additional imaging.
Preoperative planning: Imaging of donor Whole organ transplantation can be done from a deceased donor. Depending on the cause of the donor’s death, various imaging may be available. If CT images
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are available, donor anatomic variants and suitability of organs for donation can be assessed prior to organ procurement (Fig. 1). In most cases, multiple abdominal organs from a single donor are distributed to several recipients. The procurement team must separate the organs while maintaining viability, with the preservation of the major blood vessels for each donor organ to enable anastomosis into the recipient. The pancreas and liver share blood supply and drainage. Blood vessels, such as the portal vein, celiac axis branches, and sometimes replaced right hepatic artery from the superior mesenteric artery (SMA), must be divided properly so that both organs remain perfused. The celiac axis and its hepatic artery branches remain with the liver. The splenic artery, which is a branch of the celiac axis, is harvested to remain with the donor pancreas as the splenic artery supplies the pancreatic body and tail. The donor SMA is harvested to supply the donor pancreas head via its branch, the inferior pancreaticoduodenal artery (IPDA). In donors with typical anatomy, a celiac axis branch, the gastroduodenal artery (GDA), must be ligated during organ harvest. The GDA branch to the pancreas is the superior pancreaticoduodenal
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a rtery which supplies the head of the pancreas. In the donor pancreas, this part of the pancreatic head is supplied by collateral flow from the IPDA. Since the SMA gives rise to the IPDA, and the splenic artery is a branch of the celiac artery, the harvested donor pancreas has two separate arterial stumps. Usually, a Y-graft is formed from donor iliac arteries to make a common conduit for arterial blood supply the donor pancreas. Donor pancreas venous drainage is by intrapancreatic tributaries into the splenic and superior mesenteric veins (SMVs), which coalesce into the portal vein. Generally, 1–2 cm of the donor portal vein is harvested with the donor pancreas. In most cases, the majority of the donor portal vein stays with the donor liver. In order for the pancreas allograft to function, the pancreas duct must drain its digestive juices into the recipient. Rather than ligation of the duct at donor harvest, the current procurement practice is to keep the donor ductal system intact by including the segment of duodenal C-loop into which the pancreatic duct drains as part of the harvested tissue.
know the configuration of the anastomoses so that the appropriate structures are imaged (Fig. 2). The arterial anastomosis for the pancreas allograft is usually at recipient common iliac artery or external iliac artery to the transplant Y-graft conduit. The blood flows into the two limbs of the conduit. One limb supplies the pancreatic head via SMA to IPDA. The other limb supplies the pancreatic body and tail via the splenic artery. The Y-graft length is tailored for patient anatomy and may be long if the graft is placed in mid-abdomen or short if graft is placed in the lower abdomen. The donor portal vein is the conduit for the venous drainage to a recipient vein. The donor portal vein may be anastomosed to the recipient iliac vein (Fig. 2A) or the recipient IVC or the recipient SMV. In cases where the donor portal vein drains to the recipient SMV (Fig. 2B), the blood flows into the recipient’s portal system. In cases where the donor portal vein drains into the recipient’s iliac vein or IVC, the blood drains into the donor’s systemic veins. Venous drainage of a native pancreas is into the portal system, which allows the liver to metabolize the pancreatic hormones. Therefore, venous drainage of a transplant pancreas via the recipient portal system emulates native pancreas physiology and intuitively should allow better function. However, either portal or systemic venous drainage yields similar clinical results thus far.1–3 Both methods are still used. For exocrine drainage, usually the donor duodenal C-loop is anastomosed to the recipient small intestine. Various approaches can be successful. Some surgeons prefer a side-to-side anastomosis; others prefer Rouxen-Y. The pancreatic head may face cranially and be in the abdomen rather than in the anatomic pelvis. Historically, the common surgical solution for exocrine drainage was donor duodenal C-loop anastomosis to the urinary bladder with the pancreatic head oriented caudally in the recipient anatomic pelvis and tail positioned more cranially (Fig. 2C). With this surgery, the pancreatic duct drains into the urinary bladder lumen, and pancreatic excretions mix with urine. Pancreatic function can be checked with urinalysis. This approach is still used at some institutions and for some patients, especially in those who do not have a simultaneous renal transplant,3 but complications, such as chemical cystitis, urethritis, and, for males, urethral leak and stricture, are serious drawbacks.4–6 Some patients have successfully undergone surgical revision to convert from exocrine drainage via urinary bladder to exocrine drainage via bowel4, 7 (Fig. 3).
Postoperative imaging
Sonography
Multiple surgical techniques have been devised for pancreatic transplantation. To image the pancreas transplant, the technologist needs to know the location of the pancreas allograft within the recipient and may need to
Sonography is the primary imaging tool for pancreatic transplant assessment. This modality is noninvasive, uses no ionizing radiation, and can be done at the patient’s bedside. Patient body habitus, depth of
FIG. 1 Donor pancreas. The arterial supply to the tail and body is from the splenic artery (SA). The arterial supply to the head is from the inferior pancreaticoduodenal (IPDA) artery, a branch of the superior mesenteric artery (SMA). The SA and SMA stumps receive flow through a Y-graft, usually constructed from donor iliac arteries. The venous drainage from the pancreas flows into the portal vein. The donor pancreas head remains attached to a short segment of donor duodenum, into which the donor pancreatic duct (not illustrated) maintains its normal drainage.
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FIG. 2 Typical pancreas transplant anatomy. (A) Posttransplant anatomy. Transplant pancreas receives its arterial supply via Y-graft from recipient common iliac artery and drains via donor portal vein into recipient common iliac vein. The transplant pancreatic head and duodenal segment remain intact, allowing drainage of pancreatic duct. The duodenal segment is anastomosed to recipient bowel for enteric drainage. (B) Posttransplant anatomy. Transplant pancreas receives its arterial supply via Y-graft from recipient common iliac artery and drains via donor portal vein into recipient superior mesenteric vein. The transplant pancreatic head and duodenal segment remain intact, allowing drainage of pancreatic duct. The duodenal segment is anastomosed to recipient bowel for enteric drainage. (C) Posttransplant anatomy. Transplant pancreas receives its arterial supply via Y-graft from recipient common iliac artery and drains via donor portal vein into recipient common iliac vein. The transplant pancreatic head and duodenal segment remain intact, allowing drainage of pancreatic duct. The duodenal segment is anastomosed to recipient urinary bladder and the pancreatic exocrine drainage is into the urine.
the transplanted pancreas within the patient, and configuration of bowel adjacent to the pancreas determine how complete an examination is possible. Bandages and bowel gas limit visibility of the transplant, even in the hands of very skilled sonographers. Prior to obtaining images, the ultrasound technologist either reads the operative report or checks with the transplant surgeon to confirm location of the organ and to check the configuration of the vascular and enteric anastomoses. The American College of Radiology, the American Institute of Ultrasound in Medicine, the Society for Pediatric Radiology, and the Society of Radiologists in
Ultrasound have agreed upon the following indications for ultrasound examination of the transplanted pancreas8: 1. Performance of a screening ultrasound examination to establish a baseline after transplantation as per the hospital surveillance protocol; 2. Follow-up of abnormal findings on a prior transplant ultrasound examination; 3. Assessment of graft dysfunction in patients with abnormal laboratory values or clinical parameters (such as elevated blood glucose); 4. Evaluation for suspected stenosis or thrombosis of the vasculature;
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FIG. 3 Normal transplant sonogram. (A) Grayscale sonogram image shows the normal transplant pancreas (marked by calipers) with adjacent bowel and with vessels posterior to transplant. (B, C) Color Doppler and spectral Doppler of the Y-graft conduit. Note: The color scale is set so that red indicates flow toward transducer and blue indicates flow away. In (B), the transplant pancreas is outlined by a yellow dotted line and the Y-graft conduit is marked by a long yellow arrow. In (C), the spectral waveform shows a normal rapid upstroke in systole and remains above the horizontal line in diastole, indicating flow toward the transplant pancreas. (D) Color Doppler of the transplant pancreas splenic artery supplying body and tail. In the complete study, the technologist obtains a similar image of the transplant superior mesenteric artery in the pancreatic head. Also, arterial spectral waveforms are obtained at the head, the body, and the tail. (E, F) Color and spectral Doppler of the venous outflow of transplant splenic vein and transplant portal vein. The venous waveform exhibits nearly the same velocity in systole and diastole.
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5. Evaluation of pain at or near the surgical site; 6. Evaluation of the response to treatment (such as immunosuppressive therapy in the setting of rejection); 7. Evaluation for iatrogenic injury or complications after biopsy of a transplanted pancreas; and 8. Assessment of the transplant in the setting of infection or pancreatitis. The examination consists of grayscale, color Doppler, and spectral Doppler assessment. For the grayscale assessment the technologist attempts to image the entire allograft pancreas in transverse and longitudinal planes so that its size and echogenicity can be evaluated. Grayscale images are helpful for the evaluation of pancreatic duct diameter/dilatation. Once the position and orientation of the organ are defined and parenchymal images are obtained, grayscale images of the arterial Y-graft, pancreatic arterial vasculature, and donor portal vein are obtained for the evaluation of intraluminal abnormalities. The space surrounding the transplant is assessed, and if any fluid collections are visible, the technologist obtains images. For patients with enteric drainage of the pancreatic duct (the majority of US patients), imaging of any adjacent fluid-filled bowel for dilatation is performed. For patients with urinary bladder drainage of the transplant pancreatic duct, transverse and longitudinal bladder imaging is performed. If a pancreatic stent is present, the technologist attempts visualization of proximal and distal ends. The vessels assessed by Doppler are: (1) both limbs of the transplant arterial Y-graft, (2) the transplant SMA, (3) the transplant splenic artery, (4) the recipient artery (usually the common or external iliac artery), (5) the transplant SMV, (6) the transplant splenic vein, (7) the transplant portal vein, and (8) the recipient vein (usually an iliac vein or the SMV). The arterial and venous anastomoses are assessed. Vessels are assessed with color Doppler and spectral Doppler. If necessary, power Doppler is used. Color or power Doppler images of the entire pancreas transplant are obtained to assess the global vascularity of the graft. Color Doppler allows velocities to be imaged within a fairly large region of interest for the identification of presence and direction of flow. Usually, the sonographer sets the image parameters so red indicates flow toward the transducer and blue indicates flow away from the transducer. If flow velocity is too high for the settings, an artifact called aliasing, a mixture of multiple colors, appears. If color Doppler is not technically possible, such as with very low flow, power Doppler is utilized. Power Doppler detects lower velocity flow but does not show flow direction. Spectral Doppler allows a quantitative assessment of flow, represented as a waveform. The shape and size of the waveform contain information indicating velocity and direction of blood flow over a time period.
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Samples are typically obtained for several cardiac cycles. Spectral Doppler images are obtained in the following areas: (1) within the recipient artery proximal to the Y-graft anastomosis, (2) within the Y-graft itself, (3) within the transplanted pancreas splenic artery, (4) within the transplant SMA, and (5) at any areas of color flow aliasing. Doppler indices obtained at these locations include the peak systolic velocity (PSV), and may include resistive indices (RIs). The transplant veins are assessed as well. Color and spectral Doppler images of the graft splenic vein, SMV, and portal vein to the recipient venous anastomosis are obtained. Spectral Doppler assessment of the peak velocity may be performed within the graft portal vein, at the graft portal vein-recipient venous anastomosis, and distal to the anastomosis within the recipient vein. Additional measurements at areas of color flow aliasing may be helpful. Images to demonstrate venous flow in the head and tail of the transplanted pancreas are obtained. Two additional methods of ultrasound assessment of the pancreas transplant are possible but not as widely used. One is contrast-enhanced ultrasound (CEUS). With this method, contrast designed to show blood flow and perfusion is administered intravenously. The contrast is composed of biocompatible gas-filled microspheres. With contrast enhancement, the transplant pancreas perfusion can be assessed for pattern of enhancement (homogeneous, heterogenous, or areas without enhancement), and time-intensity curves can be generated.9–12 Some research has been done regarding predictability of insulin production/function of the transplant pancreas by using the CEUS generated time-intensity curves.13 The other method is scanning with Superb Microvascular Imaging technology, which can detect very slow flow with a unique algorithm designed to differentiate motion artifact or clutter from flow.14 This technique is different from power Doppler which uses a wall filter to help detect low flow.
Computed tomography and magnetic resonance imaging These modalities may be used to supplement sonography in order to more fully characterize a finding or to solve a problem when the sonogram does not show the reason for the patient’s clinical problem. With unenhanced CT (meaning no intravenous contrast), the position and size of the transplant, peri- transplant fluid collections, and bowel obstruction can be assessed. Enteric contrast is useful for bowel leak detection. With contrast-enhanced CT, the pancreas transplant enhancement pattern can be assessed, as can vascular patency. The MRI (Fig. 4) can be performed with various techniques to focus on the pancreas allograft parenchyma
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FIG. 4 MRA: (A) Contrast-enhanced delayed T2 weighted axial image reveals a diffusely enlarged swollen transplant pancreas (yellow arrows). Blood vessels appear white with this technique. (B) The processed images show patent Y-graft arterial conduit (yellow arrow) from iliac artery with intact arteries of the allograft pancreas (circled). B = bowel.
and surrounding tissue or to focus on the vasculature or on the pancreatic duct. If the patient has poor renal function and cannot tolerate intravenous contrast, unenhanced MRI shows more information about vasculature than unenhanced CT.15
Interventional imaging Pancreatic transplant biopsies are often performed with ultrasound guidance16 (Fig. 5), especially in patients who have a pancreas transplant without a kidney transplant from the same donor. Typically, if a patient has a renal transplant from the same donor, renal transplant biopsy can predict rejection of the pancreas transplant.
Ultrasound-guided pancreas transplant biopsy is part of routine care at many institutions. The pathologist needs tissue because no pathognomonic imaging studies or serum tests are available for diagnosis of graft rejection. By the time a patient develops hyperglycemia, the allograft pancreas is in later phases of rejection and the damage is usually irreversible.17 Interventional angiography is used to treat vascular complications of pancreas transplantation with options of venous thrombectomy or thrombolysis, endovascular stent grafts, and coil embolization18–20 (Fig. 9). The CT or ultrasound guidance can be helpful in drainage procedures if the patient develops fluid collections or abscess.
Complications Some complications happen early after surgery, such as anastomotic breakdown with bowel leak, hemorrhage, and infection. Other complications are more of a threat later, such as chronic rejection or posttransplantation lymphoproliferative disorders (PTLD). Length of time from surgery to clinical presentation helps determine which imaging examinations are likely to be most helpful.
Vascular complications
FIG. 5 Ultrasound guided pancreas transplant biopsy. Visualized portion of the pancreas is outlined by a yellow dotted line. The visualized portion of the biopsy needle is the oblique white line, indicated by yellow arrows.
The most common vascular complication is venous thrombosis21, 22 (Figs. 6 and 7), which occurs about twice as often as arterial thrombosis. The splenic vein stump often has a small amount of thrombus at the blind end in the transplant pancreatic tail. If this acts as a nidus and thrombus becomes more extensive, thrombus can change from an expected finding to a complication. With
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FIG. 6 Venous thrombosis, transplant failure: (A) Color Doppler image shows a swollen, heterogeneous pancreas (outlined by yellow dots) and portions of thrombosed transplant veins (outlined in green). Color does not fill the veins, and color flow is absent in the pancreatic parenchyma. (B) Power Doppler image redemonstrates the swollen, heterogeneous pancreas (outlined by yellow dots) and splenic vein (outlined in green). Only a few pixels from the power Doppler and no stream of flow are visible. (C) Doppler calipers are on splenic artery within the pancreas. Note the spectral wave form shows reversal of flow during diastole. Splenic vein (outlined in green) does not fill with color. This pancreas failed and was explanted. B = bowel, FF = free fluid.
venous obstruction the pancreas may become enlarged and edematous. On sonography, the allograft pancreas may appear hypoechogenic or heterogenous and fluid may be present around it. If the venous obstruction is due to thrombosis, the lumen of the transplant splenic vein may contain echoes. The venous Doppler signal may be absent. The arterial spectral Doppler waveform may show reversed diastolic flow, a harbinger of disaster, because it means extensive venous obstruction, with risk of transplant infarction.23 Thrombosis, arterial, venous, or combination, is called pancreatic allograft thrombosis.24 Most publications do not distinguish between arterial or venous pancreas allograft thrombosis.21, 22 Depending on severity and chronicity, thrombosis can be treated by anticoagulation, mechanical thrombectomy, or transplant pancreatectomy (also called explantation).25
Arterial thrombosis is diagnosed by absent arterial flow on color and power Doppler and absent arterial spectral waveform. Contrast-enhanced CT may be used to demonstrate extent of thrombus (Fig. 8). As noted above, if a patient cannot receive IV contrast material, unenhanced MRI is preferred over unenhanced CT. Unenhanced MRI can demonstrate increased signal on T1-weighted sequences or loss of normal flow void, permitting a diagnosis.15, 26 Contrast-enhanced CT can demonstrate the extent of venous thrombosis, which may help determine whether anticoagulation is necessary.24 Arterial pseudoaneurysm (Fig. 9) is rare, potentially life-threatening, complication20, 27 associated with intraabdominal infections before or at the time of diagnosis. The pseudoaneurysm can occur either at an anastomosis27 or in the pancreas or nearby tissues.28
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FIG. 7 Venous thrombosis, transplant survival: (A) Color Doppler image shows homogeneous pancreas (outlined by yellow dots) with thrombosed transplant splenic vein (outlined in green). Color does not fill the vein, but color flow is present within the pancreatic parenchyma. (B) Power Doppler image redemonstrates the pancreas (outlined by yellow dots) and splenic vein (outlined in green). The power Doppler shows no splenic vein flow. (C) Doppler calipers are on splenic artery within the pancreas. Note the spectral wave form shows forward flow during diastole. Splenic vein (outlined in green) does not fill with color.
An arterial pseudoaneurysm may be detected with various imaging modalities. When the “cyst” is assessed with color Doppler, a swirling “yin-yang” appearance is observed. If spectral Doppler is used to interrogate the pseudoaneurysm neck, a biphasic to-and-fro waveform is produced.29 With CT or MRI, contrast-enhanced imaging can help in characterizing a pseudoaneurysm and a larger region of the patient’s anatomy for surgical or endovascular treatment planning.28 Arterial pseudoaneurysms in the setting of pancreas allograft can be successfully treated by stent placement or surgery.20 The rare arterial pseudoaneurysm produced during a biopsy or from surgery may have an associated arteriovenous fistula.20 A procedure can also be complicated by an arteriovenous fistula without an arterial pseudoaneurysm, which may not be visible on the grayscale sonogram. When color Doppler is applied, an area of color aliasing may show at the fistula. The spectral Doppler waveform will be high-velocity, low-resistance
aveform. The arterial waveform will have increased w diastolic flow, and the venous waveform will be pulsatile. Just as with pseudoaneurysm, if an arteriovenous fistula is seen with a sonogram, a CT or an MRI is useful to show the extent and full anatomy of the complication.29 Early venous opacification and a draining vein can sometimes be demonstrated. Many small arteriovenous fistulas spontaneously resolve. Large, hemodynamically significant arteriovenous fistulas may need to be repaired.15 Arterio-enteric and arterio-urinary fistulae are rare problems, usually in grafts with chronic rejection or that no longer function.27 Patients may present with life-threatening hemorrhage.20, 27 Because any patient with clinically significant gastrointestinal hemorrhage may get an angiogram, it is critical for the angiographer to know the pancreas transplant history so that transplant angiography could be performed before mesenteric angiography. If the angiographer performs
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FIG. 8 Arterial thrombosis of Y-graft: Axial images from contrast-enhanced CT demonstrate the Y-graft (yellow arrows). (A) Proximal conduit completely fills with contrast. (B) Proximal edge of thrombus with less enhancement inside the conduit. (C) Distal end of conduit does not fill with the contrast.
the usual mesenteric angiogram, the arterio-enteric or arterio-urinary fistula could not be imaged, and the patient may continue to have hemorrhage. Either arterial or venous stenosis may be detrimental for a pancreatic transplant. These can be detected with sonography. Stenosis creates turbulent flow, which can show aliasing on color Doppler. Spectral Doppler shows increased velocity at the stricture. Note that in the immediate postoperative time period, for up to a week, perianastomotic edema may cause a temporary narrowing that resolves as the anastomosis heals, but if findings indicating stenosis do not improve or if findings indicating stenosis newly appear after the first postoperative week, CT angiography of MR angiography are performed.15 If one of these studies confirms the diagnosis, catheter angiography, and possibly therapeutic intervention, may be performed. Venous stenosis can diffuse narrowing of the transplant portal vein regardless of whether the drainage is to recipient system or portal venous system. When this happens, long-term anticoagulant therapy may be beneficial.28
Nonvascular complications Nonvascular complications include collections such as hematoma or abscess, graft-related complications of pancreatitis with pseudocyst or walled-off necrosis, and graft-related complications of rejection. Enteric complications include bowel obstruction and bowel leak. There is also a risk of tumor, such as PTLD. Postoperative hematoma A hematoma can form at the operative site after any surgery. A small hematoma that does not compress vasculature or the pancreas allograft is expected, but a large hematoma can cause problems. With ultrasound assessment, a new hematoma appears as a smoothly marginated, moderately echogenic structure without internal vascular flow. Over time, internal architecture of a hematoma becomes more complex with varying areas of fluid. Eventually, a hematoma may liquefy. On CT, the hematoma begins as a smoothly marginated, nonenhancing, hyperattenuating structure. On CT, subacute hematomas
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FIG. 9 Pancreatic graft artery pseudoaneurysm with surrounding hemorrhage: (A–D) Axial-enhanced CT images from cranial to caudal. Axial images show enlarged, heterogeneous pancreas transplant (marked by yellow arrows) that is infiltrated from hemorrhage. Blurry white areas in the pancreas are foci of hemorrhage. Major source is a large bilobed pseudoaneurysm (marked with black asterisk), arising from the transplant SA (marked by aqua arrows). Transplant SMA is marked by +. A = aorta, B = bowel, Y = Y-graft conduit. (E) Three-dimensional reconstruction. This format allows visualization of the entire contrast-enhanced vasculature at one time. In addition to the large pseudoaneurysm, areas of focal dilatation in transplant SMA and SA (marked with blue asterisk) are visible. (F, G) Angiogram with coil embolization that thrombosed the pseudoaneurysm.
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may have internal hematocrit levels, eventually becoming hypoattenuating. The appearance on MRI depends on the age of the hematoma and how much extracellular methemoglobin is present. Postoperative abscess Abscesses can occur from surgical field contamination or other predisposing problems, such as breakdown of the bowel anastomosis. They more commonly appear during the first month after surgery.15 The classic imaging appearance of an abscess is a thick-walled, complex fluid collection with internal debris or even gas. Pancreatitis All pancreas allografts have at least mild pancreatitis right after transplantation, but most often the pancreas heals without complication.30 There is a small group of patients for whom the pancreatitis is clinically important. The imaging of pancreatitis involving a transplant pancreatitis has the same features as that of a native pancreas. In early pancreatitis, the amylase and lipase are elevated, but the pancreas appears normal with imaging. Later, the pancreas becomes globular and swollen in appearance, with loss of the normal surface undulation. The sonographic appearance of acute pancreatic transplant graft rejection and pancreatitis are indistinguishable at this swollen stage.31 Biopsy can differentiate the two.17 If the pancreatitis is severe, over time the pancreas becomes heterogeneous and can become hypoechoic. Perigraft fluid is common. Regions of parenchymal flow abnormality with hyperemia adjacent to decreased flow may be apparent on color Doppler. Vascular
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c omplications of pancreatitis include splenic vein thrombosis and pseudoaneurysm. Depending on clinical circumstances, contrast- enhanced CT may be helpful for the assessment of possible pancreatitis. The CT is useful for demonstrating the location of any pancreatic duct disruption and for showing relationships between perigraft collections and bowel. The extent of gas collections are well demonstrated with CT, while ultrasound only shows diffuse “dirty” shadowing. CT enhancement patterns can show pancreatic necrosis. Rejection Rejection is classified as acute, subacute, or chronic. Historically, acute rejection was an issue. Immuno suppression therapy has decreased acute rejection, so now chronic rejection is more likely to cause graft loss than acute rejection.15, 26 Imaging findings are not specific for rejection.26 In acute rejection, the pancreas may enlarge and appear swollen.15 The transplant duodenum also appears thickened. With chronic rejection, the pancreas eventually becomes atrophic. Resistive indices are not a reliable indicator of rejection.
Bowel complications Pancreas transplant surgery involves the bowel, which imparts the risks of bowel leak and bowel obstruction. Although anastomotic leak requires immediate surgery, the leak usually does not lead to loss of the transplant pancreas.15 The best way to detect enteric leak is CT with enteric contrast (Fig. 10), but even CT without enteric contrast sometimes demonstrates signs of leak, such as gas or fluid adjacent to bowel anastomosis or new or increased pneumoperitoneum. Imaging signs of
FIG. 10 CT with enteric contrast. Patient presented with a fever, high WBC, and severe abdominal pain. (A) Coronal format demonstrates diffusely enlarged transplant pancreas (yellow arrows) and mildly thickened wall of adjacent small bowel (light blue arrows). Contrast within bowel appears bright white and any leakage into peritoneum would increase the white or brighten appearance of a fluid collection (raise the CT density). (B) Axial image of the patient’s pelvis shows free fluid that is NOT dense. This study indicates transplant pancreas pathology, not bowel leak, is the problem. B = bowel.
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bowel obstruction can be seen on a radiographic abdominal series, but CT is often better for the visualization of a transition zone from distended to decompressed caliber bowel. Adhesions and internal hernia are two potential etiologies of obstruction.30
Posttransplant lymphoid proliferative disorders Posttransplant lymphoid proliferative disorders (PTLD) are a group of related lymphatic system disorders, ranging from benign B-cell hyperplasia to lymphoma.32 These disorders are a complication of chronic immunosuppression, found less frequently in patients who have tacrolimus as part of the immunosuppression than in patients who are not on tacrolimus.33 Recipients who are Epstein-Barr virus-negative have an increased risk of developing PTLD, especially after exposure to Epstein-Barr virus.33 Symptoms of PTLD are nonspecific, such as fevers, chills, malaise, nausea, and vomiting.34 Imaging of patients with these symptoms often includes an abdominal CT scan. With PTLD of the pancreas, diffuse pancreas enlargement (more common) or a focal pancreatic mass, often in the head, may be present.34 Numerous small intraabdominal lymph nodes may be visible.34 Some patients present with involvement of other organs with no graft involvement34 (Fig. 11). Just as the symptoms, the imaging findings are nonspecific. If present, enlarged lymph nodes point toward PTLD rather than rejection or pancreatitis. Ultrasound-guided biopsy is helpful for differentiating the process present. Although only about 1% of pancreas transplant patients develop PTLD,33 the correct diagnosis is critical because treatment is the opposite of therapy for rejection. The treatment for PTLD is immune system stimulation.
FIG. 11 Metastatic PTLD. Chest radiograph of patient who became infected with EBV and CMV after her transplant. In addition to pulmonary nodules, she had liver lesions and mildly enlarged abdominal lymph nodes. The transplant pancreas was not enlarged.
Conclusion Imaging of the pancreas transplant patient is valuable for sorting out complications that have similar clinical presentations. An understanding of the particular surgical anatomy is critical for optimal imaging assessment. Sonography is used for routine evaluation of the allograft and its vasculature. If sonography is limited or if complications are only partly visualized or not well assessed with this modality, CT is beneficial for assessing complications outside the pancreatic graft itself, such as bowel obstruction or leak. If a patient cannot tolerate intravenous contrast, MR is an excellent method to visualize vasculature and duct. Interventional imaging is of assistance for this patient population, with ultrasound-guided biopsy being most common. Other procedures, such as image-guided fluid aspiration or abscess drainage and diagnostic and therapeutic angiography procedures, can improve the clinical course if the patient has a complication.
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