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Management of vascular and nonvascular complications following pancreas transplantation with interventional radiology
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Diagnostic and Interventional Imaging (2020) xxx, xxx—xxx
REVIEW
Management of vascular and nonvascular complications following pancreas transplantation with interventional radiology A. David a,∗, E. Frampas a, F. Douane a, C. Perret a, F. Leaute a, D. Cantarovich b, G. Karam c, J. Branchereau c a
Department of Radiology, Nantes University Hospital, University of Medicine of Nantes, 44093 Nantes, France b Department of Nephrology, Nantes University Hospital, University of Medicine of Nantes, 44093 Nantes, France c Department of Urology, Nantes University Hospital, University of Medicine of Nantes, 44093 Nantes, France
KEYWORDS Pancreas transplantation; Postoperative complications; Radiology; Interventional; Endovascular procedures; Arteriovenous fistula
Abstract Pancreas transplantation exposes to high rates of complications, either vascular (thrombosis, stenosis, pseudoaneurysm, arteriovenous fistula) or nonvascular (fluid collection, graft rejection). With advances in percutaneous and endovascular techniques, interventional radiologists are increasingly involved in the management of these complications. In this article, we review the anatomical considerations relevant to pancreas transplantation, the techniques used for image-guided interventions for vascular and nonvascular complications, and the expected outcomes of these interventions. © 2020 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
∗ Corresponding author. Department of Radiology, Centre Hospitalier Universitaire de Nantes, 1, place Alexis-Ricordeau, 44093 Nantes cedex 1, France. E-mail address: [email protected] (A. David).
Pancreas transplantation is a well-established therapeutic option for patients with severe type 1 insulin-dependent diabetes, offering long-term graft survival rates of up to 85% at 1 year [1]. However, pancreas transplantation is a major undertaking, exposing to higher rates of complications than other solid organ transplantations. Indeed, the need for repeat laparotomy is up to 43% of patients, which significantly impairs graft survival [2]. Technical complications (vascular, infectious, pancreatitis) represent more than 50%
https://doi.org/10.1016/j.diii.2020.02.002 2211-5684/© 2020 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
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of early graft failure (within 6 months from transplantation) and less than 10% of late graft failure (after 6 months from transplantation) [3]. With recent advances in percutaneous and endovascular techniques, interventional radiologists are increasingly involved in the management of these vascular and nonvascular complications. The general principles of endovascular management of vascular complications are based on thrombolysis and thrombectomy for thrombosis [4—8], transluminal angioplasty for stenosis [8—10] and embolization for pseudoaneurysms, arterio-enteric fistulae and arteriovenous fistulae (AVF) [11—23]. Nonvascular complications after pancreas transplantations include peripancreatic fluid collections, graft pancreatitis, intestinal complications (leak and obstruction), graft rejection and post-transplantation lymphoproliferative disorder. In this review, we will mainly focus on fluid collections, for which image-guided drainage is frequently useful [24] and graft rejection, confirmed by percutaneous biopsy [25]. The purpose of this article is to provide an overview of image-guided interventions related to vascular and extravascular complications occurring after pancreas transplantation.
Surgical and anatomical considerations of simultaneous pancreas—kidney transplantation Approximately 80% of pancreas transplantations are simultaneous pancreas—kidney transplantations, with surgical complication rates similar to those of pancreas after kidney transplantations and solitary pancreas transplantations [26]. The pancreas is harvested with its native arterial and venous blood supply and with a variable portion of the donor duodenum C-loop [27]. Pancreas transplants are most commonly placed into the recipient’s right iliac fossa or pelvis. Pancreas transplant’s arterial supply is commonly via a vascular reconstruction known as ‘‘Y-graft’’, consisting of the donor common iliac artery, external and internal iliac artery branches. The donor common iliac artery is anastomosed end-to-side to the recipient common iliac artery, while the donor external and internal iliac arteries are anastomosed end-to-end to the donor splenic (supplying pancreas body and tail) and superior mesenteric arteries (supplying pancreas head) (Fig. 1). Pancreas transplant venous drainage is provided by the donor portal vein that is harvested with the donor mesenteric and splenic veins. The allograft portal vein can either be anastomosed to the recipient common iliac vein or inferior vena cava (systemic drainage) or to the recipient superior mesenteric vein (portal drainage) (Fig. 1). Pancreatic exocrine secretions were originally drained to the bladder via a duodenocystotomy but inflammatory complications due to pancreatic enzymes were reported [28,29]. Most of pancreas transplantations are now performed by using an enteric drainage via a duodenojejunostomy (Fig. 1). The donor duodenum is then anastomosed to the recipient small bowel through a side-to-side anastomosis or a Roux-en-Y anastomosis.
Noninvasive imaging Noninvasive imaging plays a central role in the postoperative management of patients with pancreas transplantation. Ultrasound with duplex and color Doppler imaging is useful in the detection of vascular complications or peritransplant fluid collections, but can be limited by overlying bowel gas [30]. Computed tomography (CT) and magnetic resonance imaging (MRI) are both useful tools to evaluate the allograft ant its vascular supply, and have similar performances for the detection of vascular abnormalities (Fig. 2) [31]. Nevertheless, CT provides several advantages compared to MRI in the postoperative period, despite its irradiating nature and the need for intravenous administration of iodinated contrast material. Indeed, CT is usually more available in emergency situations and allows for a rapid exploration of the whole abdomen [32]. Optimal evaluation of the graft and its vascular supply require a multiphasic CT acquisition, with unenhanced phase followed by arterial and venous phases, especially in the potentially life-threatening setting of vascular complications [33]. Detection and localization of a bleeding site or a vascular thrombosis is indeed crucial in order to decide on adequate medical, endovascular or surgical management. Furthermore, the use of metal artifact reduction algorithm may be useful for patients with repeat bleeding after previous embolization with metallic coil [34].
Vascular complications Vascular complications include vessel thrombosis, stenosis, pseudoaneurysm/arterio-enteric fistula, and AVF. They are usually associated with hyperglycemia, increased insulin demands and graft tenderness.
Thrombosis Affecting 5% to 14% of pancreas transplantation [33], graft thrombosis is the second overall cause of graft failure after rejection, being responsible for 2.7% to 8% of graft loss [35]. Venous thrombosis is more frequent than arterial thrombosis, with an approximate 2:1 ratio, and may result from changes in hemodynamic of the pancreatic transplant splenic vein due to the loss of splenic circulation. The most common risk factors of graft thrombosis are hypoperfusion, surgical technical issues, sepsis, immunosuppression and prolonged graft ischemia [36]. There is no consensus for antithrombotic medication in prevention of graft thrombosis but many authors use systemic anticoagulation associated or not with antiplatelet agents during the immediate postoperative course [37]. A close glycemic control must be applied, with early Doppler or CT examination when a thrombosis is suspected. The ultrasound Doppler findings of venous thrombosis include absence of venous flow, high resistive indices and reversal of diastolic flow in transplant arteries [38]. On CT examination, the thrombus is usually spontaneously hyper-attenuating, with a mean attenuation value of 42 Hounsfield units, and presents as a filling defect after intravenous administration of iodinated contrast material [39,40]. Management of venous graft thrombosis is challenging. Immediate
Please cite this article in press as: David A, et al. Management of vascular and nonvascular complications following pancreas transplantation with interventional radiology. Diagnostic and Interventional Imaging (2020), https://doi.org/10.1016/j.diii.2020.02.002
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Figure 1. Schematic illustration of a pancreas transplant with systemic venous drainage and enteric exocrine drainage. Arterial supply is provided by a Y-graft connected to donor superior mesenteric and splenic arteries, and anastomosed to the recipient common iliac artery. Venous drainage uses the donor portal vein anastomosed to the recipient inferior vena cava. Exocrine secretions are drained to the recipient small bowel via the donor duodenum C-loop using a duodenojejunostomy.
Figure 2. Normal computed tomography appearance of pancreas graft 10 days after solitary pancreas transplantation a 35-year-old man: a: contrast-enhanced computed tomography image in a coronal oblique plane shows the pancreas transplant (star) with the duodenal C-loop (arrowheads) sited within the right iliac fossa; b: contrast-enhanced computed tomography image with maximal intensity projection in a coronal oblique plane shows the anastomoses between donor portal vein and recipient inferior vena cave (white arrow) and between donor Y-graft and recipient common iliac artery (black arrow).
reoperations, such as surgical thrombectomy, are mandatory in patients with complete parenchymal necrosis. However, in the absence of graft necrosis, surgery often fails to obtain graft salvage [41]. Moreover, they require general anesthesia and expose to high postoperative morbidity and mortality rates [42]. Systemic anticoagulation therapy is often sufficient in partial venous graft, preventing the propagation of the thrombus, but may be ineffective for extensive luminal obstruction [43]. Endovascular interventions may have a role
in the treatment of these venous thromboses in the absence of parenchymal necrosis [4—8]. They include transarterial thrombolysis, mechanical thrombectomy, thrombus angioplasty or catheter-directed-thrombolysis with aspiration thrombectomy. A successful transarterial thrombolysis was reported by Yoshimatsu et al. but this technique results in a delayed recanalization and requires high doses of urokinase [4]. Mechanical thrombectomy and thrombus angioplasty using an inflated-balloon catheter has been described in one
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Figure 3. 34-year-old woman with graft venous thrombosis 19 days after simultaneous pancreas—kidney transplantation: a: contrastenhanced computed tomography image in the coronal plane shows a defect within the pancreatic graft portal vein (arrow) and pancreatic edema (star); b: initial pancreatic graft portal venography performed via a right femoral vein approach, confirms presence of proximal thrombosis (arrow); c: fluoroscopy image shows thrombus angioplasty using a 10-mm diameter inflated-balloon catheter; d: final pancreatic graft portal venography shows significant restoration of venous outflow.
patient by Izaki et al., allowing graft salvage, but carries the risk of venous anastomosis injury (Fig. 3) [5]. Percutaneous endovenous thrombolysis with aspiration thrombectomy is the most reported technique [6—8,35]. Barrufet et al. have evaluated 17 patients, and reported patient and pancreas graft survival rates at 12 months of 94 and 76%, respectively, without any procedure-related complication [7]. By comparison, a graft salvage rate of 45% was reported by Fridell et al. using surgical thrombectomy [42]. Usually through a venous femoral access, the splenic and mesenteric veins are directly catheterized, preferably with a dedicated hydrodynamic mechanical thrombectomy device. The thrombus can then be removed, with or without prior injection of a chemical thrombolytic therapy. Immediate restoration of venous flow is confirmed by a final venography (Fig. 4). Some authors have also reported the use of metallic stents for residual thrombus or anastomotic kinking or stenosis [35]. Arterial thrombosis is less frequent than venous thrombosis but their actual incidence is not well known. Arterial thrombosis conveys a poor prognosis. Some authors have attempted to treat arterial thrombosis by catheterdirected-thrombolysis, with discouraging results, probably due to the small size of pancreatic vessels [8].
Arterial stenosis Arterial stenosis has a reported incidence of 2.5%, commonly occurs during the early postoperative period and usually at anastomotic sites [33,44]. Ultrasound Doppler findings include increased velocities and turbulent flow at the anastomotic site. The diagnosis can be confirmed with CT. Investigation of vascular stenosis is possible using MRI but may be affected by surgical clips related to transplantation surgery [33]. Arterial stenosis may lead to pancreatic ischemia, in particular in patients with a low iliac inflow because of an underlying atherosclerotic disease. Percutaneous transluminal angioplasty seems to be a suitable therapeutic option for persistent stenosis with hemodynamic consequences [8—10]. The benefits of stent placement in these situations is difficult to evaluate clinically due to limited literature data but should be discussed by analogy with transplant renal artery stenosis [43].
Pseudoaneurysm and arterio-enteric fistulae Hemorrhagic complications are among the most lifethreatening complications following pancreas transplantation. With an estimated prevalence of 2.4% [45], they
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Figure 4. 53-year-old man with graft venous thrombosis 3 days after solitary pancreas transplantation: a: contrast-enhanced computed tomography image in the coronal plane shows a sub-occlusive thrombus within the pancreatic graft portal vein, involving splenic and superior mesenteric veins and extending to the inferior vena cava (arrow); b: initial pancreatic graft portal venography via a right femoral approach, confirms the presence of a nearly occlusive thrombus (arrow); c: transcatheter thrombolysis was performed using urokinase injected through a 5-F pigtail catheter, associated with aspiration thrombectomy through a 7-Fr guiding sheath. Final pancreatic graft portal venography shows a marked restauration of portal flow; d: follow-up contrast-enhanced computed tomography image I the coronal plane obtained 2 months after thrombolysis shows a nearly fully patent portal vein (arrow) with normal parenchymal enhancement of pancreatic transplant.
include pseudoaneurysms and arterio-enteric fistulae. As for bleeding in patients with native pancreas, interventional radiology plays a role in the management of these complications [46]. Pseudoaneurysms most commonly occur at transplant splenic and superior mesenteric artery anastomoses [47]. They may result from surgical technique, biopsy, infection or pancreatitis [33,48]. Transplant pancreatic artery pseudoaneurysm are often asymptomatic, but can also cause graft dysfunction or potentially lifethreatening hemorrhage [48,49]. On Doppler ultrasound, a pseudoaneurysm presents as an anechoic structure, with a characteristic bidirectional internal flow (i.e., the so-called ‘‘yin-yang’’ appearance). Cross-sectional imaging shows pseudoaneurysms as saccular lesions arising from the injured vessel, enhancing similarly to other arteries after injection of contrast material. Treatment of pseudoaneurysms is necessary because of the risk of graft dysfunction or life-threatening bleeding [50,51]. An endovascular approach is suitable for hemodynamically stable patients, including transcatheter embolization and/or covered stent placement. Embolization may be performed with various embolic materials, such as coils, plugs, detachable balloons or glue [8,11], but exposes to allograft or bowel necrosis in these end arteries. Stent-graft placement must be considered for pseudoaneurysms arising from larger arteries, typically iliac
vessels involved in the anastomosis (Fig. 5) [13]. Results from the literature, mainly based on case reports and small studies, suggests that endovascular management of pseudoaneurysms is usually feasible with rare losses of graft function but a relatively high complication rate (33.3%) [12—14]. In infected pseudoaneurysms arising from iliac vessels, stent grafting may still be considered, with low incidence of stent infection [15], but surgical resection of the aneurysm is often required for associated peripancreatic abscess. Rupture of a pseudoaneurysm in the duodenum C-loop used for enteric drainage of pancreas transplants is known as arterio-enteric fistula. This is a rare but life-threatening condition, due to the risk of major gastrointestinal bleeding. As for pseudoaneurysms, interventional radiology can play a role in the management of arterioenteric fistula, especially for patients at high surgical risk. Endovascular exclusion of the fistula may be performed using transcatheter embolization with coils, particles or glue, or using covered stenting of the involved artery [12,16,17].
AVF AVF is a rare complication of pancreas transplantation, with an estimated incidence of 1.4% [52]. AVF may result
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Figure 5. 36-year-old woman with hemorrhagic shock and arterial pseudoaneurysm 10 days after pancreas graft explantation: a: contrastenhanced abdominal computed tomography image with maximal intensity projection in the coronal plane shows large pseudoaneurysm (arrow) arising at site of previous end-to-side anastomosis; b: initial digital subtraction angiogram via a right femoral approach confirms the presence of a pseudoaneurysm (star) arising at site of previous end-to-side anastomosis (arrow); c: endovascular treatment was performed by placing 13.5 × 40 mm iliac covered stent-graft (Fluency® , Bard). Final angiogram shows complete exclusion of the pseudoaneurysm by the covered stent (between arrowheads).
Figure 6. 42-year-old man presenting with an asymptomatic arteriovenous fistula 2 months after simultaneous pancreas—kidney transplantation: a: color Doppler ultrasound shows pulsatile arterialized flow in the draining vein, suggesting pancreas graft arteriovenous fistula; b: contrast-enhanced computed tomography image in the coronal plane during the arterial phase shows early opacification of the portal vein (PV) through an arteriovenous fistula (arrow) fed by the pancreas graft superior mesenteric artery (SMA); c: initial digital subtraction angiogram of pancreatic graft via a right femoral approach shows early venous drainage (arrow) confirming the presence of a large arteriovenous fistula (PV: portal vein; SMA: superior mesenteric artery); d: angiogram shows superior mesenteric arterial feeder supplying the arteriovenous fistula that was embolized using a 10-mm Amplatzer® vascular plug (AGA Medical Corp.) (between arrowheads). Postembolization angiography confirms occlusion of arteriovenous fistula and no further opacification of the early draining vein.
from the postoperative (blind ligation or surgical stapler) or post-biopsy laceration of both arterial and venous walls. AVF can be seen either on transplant mesenteric root (superior mesenteric vessels) or on pancreatic tail (splenic vessels). Persistent AVF may potentially lead to major bleeding or graft loss if untreated [53,54]. Doppler ultrasound shows focal aliasing with a high velocity, low-resistance
arterial inflow and a pulsatile arterialized draining vein [54]. Cross-sectional imaging may show enlarged Y-graft arteries with an early opacification of the donor draining vein during arterial phase [48]. Transcatheter angiography remains the gold standard for the diagnosis of AVF, showing dynamic images and allowing for endovascular treatment [18]. Persistent and/or symptomatic large AVF
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Figure 7. 45-year-old man peripancreatic fluid collection 9 days after simultaneous pancreas—kidney transplantation: a: contrastenhanced abdominal computed tomography image in the axial plane shows well-defined fluid collection (star) around the pancreas transplant with peripheral rim enhancement (arrowheads); b: percutaneous drainage was performed using a 12-Fr drainage catheter (Cook) inserted under computed tomography guidance through an anterior approach. Due to the presence of Candida albicans in the fluid content, fluconazole was given during 6 weeks with a daily dose of 400 mg. The catheter was removed 1 month later; c: follow-up computed tomography image in the axial plane obtained 4 months later shows no residual fluid collection.
Figure 8. 53-year-old man with suspected graft rejection 14 days after solitary pancreas transplantation: a: contrast-enhanced abdominal computed tomography image in the axial plane shows mild enlargement of pancreas transplant (star) with slightly heterogenous enhancement; b: percutaneous biopsy was performed under real-time ultrasound guidance, using an 18-Gauge biopsy needle (arrow) advanced into the pancreas transplant (star). Histopathologic analysis of tissue sample confirmed acute cellular rejection.
must be treated, either by surgical or endovascular approach [19,53]. However, surgical ligation of pancreatic transplants AVF has been abandoned progressively, in favor of much less invasive transcatheter embolization [19]. Large occlusive materials, including coils, detachable balloons and plugs, should be used, as liquid embolic agents may result in allograft ischemia and/or nontarget embolization (Fig. 6) [19—23].
Extravascular complications Peripancreatic fluid collections The development of fluid collections adjacent to pancreas transplants has an estimated incidence of 11% to 16% [55,56]. Their presence is associated with a lower pancreas graft survival rate and a greater incidence of infection by comparison with patients without fluid collection (68% and 75% vs. 85% and 46%, respectively) [55]. Fluid collections may complicate intestinal leakage, pancreatitis, open lymphatics, hemorrhage or infection. They can be encountered in the early or late postoperative course following transplantation. Collections appear hypoechoic on ultrasound, except for hematomas and some abscesses that may contain
internal echoes [33]. CT shows hypo-attenuating welldefined lesions, while hematomas have hyper-attenuating content. A peripheral rim enhancement may be seen in abscesses or superinfected collections [55]. MRI may help identify hemorrhagic content because fresh blood displays hypersignal on T1-weighted images [57]. In particular, patients for whom differentiation between graft pancreatitis and leakage from the anastomosis is difficult, the use of secretin-stimulated MRI may be valuable by showing active pancreatic fistula filling the collection [58]. Percutaneous ultrasound or CT-guided needle-aspiration may be useful for further biochemical and bacteriological analysis. Up to 80% of fluid collections can be managed conservatively with percutaneous drainage [24]. Reintervention is only needed for anastomotic leakage in patients with enteric drainage, failure of conservative treatment or for hemodynamically unstable patients [24]. Percutaneous drainage can be performed either under ultrasound or CT guidance, depending on the location of the collection and operator’s preference (Fig. 7). There is no consensus regarding the size of the drainage catheter or the duration of drainage in this indication. In our experience, we routinely use 8- to 14-Fr caliber catheter, depending on the nature of the fluid, and a drainage duration of 7 to 10 days is usually sufficient before catheter removal.
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Graft rejection Despite the continuous advances in the field of immunosuppressive therapies, pancreas transplant rejection remains the first cause of graft loss after one year, with rates varying between 5% and 25% [59]. Rejection may occur immediately (hyperacute), 1 week to 3 months post-transplant (acute) or after months post-transplant (chronic). Imaging findings of rejection are non-specific, the main differential diagnosis being graft pancreatitis. At ultrasound, acute rejection presents as graft enlargement and increased parenchymal heterogeneity. Duplex and color Doppler ultrasound are also useful to exclude thrombosis. CT may show gland enlargement with heterogenous enhancement and occasionally peripancreatic fluid collections [33]. On MRI, in patients with acute rejection, pancreatic graft is hyperintense on T2weighted images due to parenchymal edema and pancreas enhancement is often altered as on CT. Chronic rejection usually results in atrophy of pancreatic graft and MRI may show decreased signal of the pancreas transplant on T1- and T2-weighted images [60]. Although rejection may be suspected on ultrasound, CT or MRI, final diagnosis and grading of both acute and chronic rejection require histopathological analysis [61]. The most common method for obtaining tissue sample is percutaneous biopsy using 18-Gauge automatic biopsy needles [25]. Ultrasound is often sufficient for guidance, offering radiation-free and real-time monitoring (Fig. 8) [25]. CT guidance may be necessary when bowel gas interposition obscures the anterior approach. According to Atwell et al., adequate allograft pancreatic tissue can be obtained with percutaneous needle biopsy in more than 96% of procedures, with less than 3% of biopsies resulting in major complications [25].
Conclusion Pancreas transplantation is a complex surgical intervention, exposing vulnerable patients to a large variety of vascular and nonvascular complications. Interventional radiologists should be familiar with pancreas transplant anatomy and surgical techniques in order to play a key role in the diagnosis and management of these complications, potentially improving outcomes for patients.
Disclosure of interest
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The authors declare that they have no competing interest.
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9 [40] Canellas R, Mehrkhani F, Patino M, Kambadakone A, Sahani D. Characterization of portal vein thrombosis (neoplastic versus bland) on CT images using software-based texture analysis and thrombus density (Hounsfield units). AJR Am J Roetgenol 2016;207:W81—7. [41] Harbell JW, Morgan T, Feldstein VA, Roll GR, Posselt A, Kang SM, et al. Splenic vein thrombosis following pancreas transplantation: identification of factors that support conservative management. Am J Transplant 2017;17:2955—62. [42] Fridell JA, Mangus RS, Mull AB, Taber TE, Sanders CE, Slisher RC, et al. Early reexploration for suspected thrombosis after pancreas transplantation. Transplantation 2011;91(8):902—7. [43] Macchini M, Mokrane T, Darcourt J, Bellière J, Kamar N, Candelari R, et al. Percutaneous transluminal angioplasty alone versus stent placement for the treatment of transplant renal artery stenosis. Diagn Interv Imaging 2019;100:493—502. [44] Khubutia MS, Pinchuk AV, Dmitriev IV, Balkarov AG, Storozhev RV, Anisimov YA. Surgical complications after simultaneous pancreas—kidney transplantation: a single-center experience. Asian J Surg 2016;39:232—7. [45] Sutherland DER. Lessons learned from more than 1000 pancreas transplants at a single institution. Ann Surg 2001;122:463—501. [46] Lee NJ, Shin JH, Lee SS, Park DH, Lee SK, Yoon HK. Transcatheter arterial embolization for iatrogenic bleeding after endoscopic ultrasound-guided pancreaticobiliary drainage. Diagn Interv Imaging 2018;99:717—24. [47] Heller MT, Hattoum A. Kidney-pancreas transplantation: assessment of key imaging findings in the acute setting. Emerg Radiol 2012;19:527—33. [48] Dillman JR, Elsayes KM, Bude RO, Platt JF, Francis IR. Imaging of pancreas transplants: postoperative findings with clinical correlation. J Comput Assit Tomogr 2009;33:609—17. [49] Lubezky N, Goykhman Y, Nakache R, Kessler A, Baruch R, Katz P, et al. Early and late presentations of graft arterial pseudoaneurysm following pancreatic transplantation. World J Surg 2013;37:1430—7. [50] Tan M, Di Carlo A, Stein LA, Cantarovich M, Tchervenkov JI, Metrakos P. Pseudoaneurysm of the superior mesenteric artery after pancreas transplantation treated by endovascular stenting. Transplantation 2001;72:336—8. [51] Surowiecka-Pastewka A, Matejak-Górska M, Fraczek M, Sklinda K, Walecki J, Durlik M. Endovascular interventions in vascular complications after simultaneous pancreas and kidney transplantations: a single-center experience. Ann Transplant 2019;24:199—207. [52] Bratton CF, Hamid A, Selby JB, Baliga PK. Case report: gastrointestinal hemorrhage caused by a pancreas transplant arteriovenous fistula with large pseudoaneurysm 9 years after transplantation. Transplant Proc 2011;43:4039—43. [53] Lowell JA, Bynon JS, Stratta RJ, Taylor RJ. Superior mesenteric arteriovenous fistula in vascularized whole organ pancreatic allografts. Surg Gynecol Obstet 1993;177:254. [54] Low G, Crockett AM, Leung K, Walji AH, Patel VH, Shapiro AM, et al. Imaging of vascular complications and their consequences following transplantation in the abdomen. Radiographics 2013;33:633—52. [55] Singh RP, Vrakas G, Hayek S, Hayek S, Anam S, Aqueel M, et al. Clinically significant perpancreatic fluid collections after simultaneous pancreas—kidney transplantation. Transplantation 2013;95:1263—9. [56] Knox J, Watson E, Fidelman N, Taylor AG, Kolli K, Lehrman E, et al. Outcomes after peripancreatic fluid drainage in patients with simultaneous pancreas—kidney transplantation. J Vasc Interv Radiol 2019;30:918—21. [57] Voutsinas N, Singh AP, Lewis S, Rosen A. Multi-modality imaging evaluation of the whole-organ pancreas transplant. Curr Probl Diagn Radiol 2019;48:289—97.
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REVIEW
Management of vascular and nonvascular complications following pancreas transplantation with interventional radiology A. David a,∗, E. Frampas a, F. Douane a, C. Perret a, F. Leaute a, D. Cantarovich b, G. Karam c, J. Branchereau c a
Department of Radiology, Nantes University Hospital, University of Medicine of Nantes, 44093 Nantes, France b Department of Nephrology, Nantes University Hospital, University of Medicine of Nantes, 44093 Nantes, France c Department of Urology, Nantes University Hospital, University of Medicine of Nantes, 44093 Nantes, France
KEYWORDS Pancreas transplantation; Postoperative complications; Radiology; Interventional; Endovascular procedures; Arteriovenous fistula
Abstract Pancreas transplantation exposes to high rates of complications, either vascular (thrombosis, stenosis, pseudoaneurysm, arteriovenous fistula) or nonvascular (fluid collection, graft rejection). With advances in percutaneous and endovascular techniques, interventional radiologists are increasingly involved in the management of these complications. In this article, we review the anatomical considerations relevant to pancreas transplantation, the techniques used for image-guided interventions for vascular and nonvascular complications, and the expected outcomes of these interventions. © 2020 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
∗ Corresponding author. Department of Radiology, Centre Hospitalier Universitaire de Nantes, 1, place Alexis-Ricordeau, 44093 Nantes cedex 1, France. E-mail address: [email protected] (A. David).
Pancreas transplantation is a well-established therapeutic option for patients with severe type 1 insulin-dependent diabetes, offering long-term graft survival rates of up to 85% at 1 year [1]. However, pancreas transplantation is a major undertaking, exposing to higher rates of complications than other solid organ transplantations. Indeed, the need for repeat laparotomy is up to 43% of patients, which significantly impairs graft survival [2]. Technical complications (vascular, infectious, pancreatitis) represent more than 50%
https://doi.org/10.1016/j.diii.2020.02.002 2211-5684/© 2020 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
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of early graft failure (within 6 months from transplantation) and less than 10% of late graft failure (after 6 months from transplantation) [3]. With recent advances in percutaneous and endovascular techniques, interventional radiologists are increasingly involved in the management of these vascular and nonvascular complications. The general principles of endovascular management of vascular complications are based on thrombolysis and thrombectomy for thrombosis [4—8], transluminal angioplasty for stenosis [8—10] and embolization for pseudoaneurysms, arterio-enteric fistulae and arteriovenous fistulae (AVF) [11—23]. Nonvascular complications after pancreas transplantations include peripancreatic fluid collections, graft pancreatitis, intestinal complications (leak and obstruction), graft rejection and post-transplantation lymphoproliferative disorder. In this review, we will mainly focus on fluid collections, for which image-guided drainage is frequently useful [24] and graft rejection, confirmed by percutaneous biopsy [25]. The purpose of this article is to provide an overview of image-guided interventions related to vascular and extravascular complications occurring after pancreas transplantation.
Surgical and anatomical considerations of simultaneous pancreas—kidney transplantation Approximately 80% of pancreas transplantations are simultaneous pancreas—kidney transplantations, with surgical complication rates similar to those of pancreas after kidney transplantations and solitary pancreas transplantations [26]. The pancreas is harvested with its native arterial and venous blood supply and with a variable portion of the donor duodenum C-loop [27]. Pancreas transplants are most commonly placed into the recipient’s right iliac fossa or pelvis. Pancreas transplant’s arterial supply is commonly via a vascular reconstruction known as ‘‘Y-graft’’, consisting of the donor common iliac artery, external and internal iliac artery branches. The donor common iliac artery is anastomosed end-to-side to the recipient common iliac artery, while the donor external and internal iliac arteries are anastomosed end-to-end to the donor splenic (supplying pancreas body and tail) and superior mesenteric arteries (supplying pancreas head) (Fig. 1). Pancreas transplant venous drainage is provided by the donor portal vein that is harvested with the donor mesenteric and splenic veins. The allograft portal vein can either be anastomosed to the recipient common iliac vein or inferior vena cava (systemic drainage) or to the recipient superior mesenteric vein (portal drainage) (Fig. 1). Pancreatic exocrine secretions were originally drained to the bladder via a duodenocystotomy but inflammatory complications due to pancreatic enzymes were reported [28,29]. Most of pancreas transplantations are now performed by using an enteric drainage via a duodenojejunostomy (Fig. 1). The donor duodenum is then anastomosed to the recipient small bowel through a side-to-side anastomosis or a Roux-en-Y anastomosis.
Noninvasive imaging Noninvasive imaging plays a central role in the postoperative management of patients with pancreas transplantation. Ultrasound with duplex and color Doppler imaging is useful in the detection of vascular complications or peritransplant fluid collections, but can be limited by overlying bowel gas [30]. Computed tomography (CT) and magnetic resonance imaging (MRI) are both useful tools to evaluate the allograft ant its vascular supply, and have similar performances for the detection of vascular abnormalities (Fig. 2) [31]. Nevertheless, CT provides several advantages compared to MRI in the postoperative period, despite its irradiating nature and the need for intravenous administration of iodinated contrast material. Indeed, CT is usually more available in emergency situations and allows for a rapid exploration of the whole abdomen [32]. Optimal evaluation of the graft and its vascular supply require a multiphasic CT acquisition, with unenhanced phase followed by arterial and venous phases, especially in the potentially life-threatening setting of vascular complications [33]. Detection and localization of a bleeding site or a vascular thrombosis is indeed crucial in order to decide on adequate medical, endovascular or surgical management. Furthermore, the use of metal artifact reduction algorithm may be useful for patients with repeat bleeding after previous embolization with metallic coil [34].
Vascular complications Vascular complications include vessel thrombosis, stenosis, pseudoaneurysm/arterio-enteric fistula, and AVF. They are usually associated with hyperglycemia, increased insulin demands and graft tenderness.
Thrombosis Affecting 5% to 14% of pancreas transplantation [33], graft thrombosis is the second overall cause of graft failure after rejection, being responsible for 2.7% to 8% of graft loss [35]. Venous thrombosis is more frequent than arterial thrombosis, with an approximate 2:1 ratio, and may result from changes in hemodynamic of the pancreatic transplant splenic vein due to the loss of splenic circulation. The most common risk factors of graft thrombosis are hypoperfusion, surgical technical issues, sepsis, immunosuppression and prolonged graft ischemia [36]. There is no consensus for antithrombotic medication in prevention of graft thrombosis but many authors use systemic anticoagulation associated or not with antiplatelet agents during the immediate postoperative course [37]. A close glycemic control must be applied, with early Doppler or CT examination when a thrombosis is suspected. The ultrasound Doppler findings of venous thrombosis include absence of venous flow, high resistive indices and reversal of diastolic flow in transplant arteries [38]. On CT examination, the thrombus is usually spontaneously hyper-attenuating, with a mean attenuation value of 42 Hounsfield units, and presents as a filling defect after intravenous administration of iodinated contrast material [39,40]. Management of venous graft thrombosis is challenging. Immediate
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Figure 1. Schematic illustration of a pancreas transplant with systemic venous drainage and enteric exocrine drainage. Arterial supply is provided by a Y-graft connected to donor superior mesenteric and splenic arteries, and anastomosed to the recipient common iliac artery. Venous drainage uses the donor portal vein anastomosed to the recipient inferior vena cava. Exocrine secretions are drained to the recipient small bowel via the donor duodenum C-loop using a duodenojejunostomy.
Figure 2. Normal computed tomography appearance of pancreas graft 10 days after solitary pancreas transplantation a 35-year-old man: a: contrast-enhanced computed tomography image in a coronal oblique plane shows the pancreas transplant (star) with the duodenal C-loop (arrowheads) sited within the right iliac fossa; b: contrast-enhanced computed tomography image with maximal intensity projection in a coronal oblique plane shows the anastomoses between donor portal vein and recipient inferior vena cave (white arrow) and between donor Y-graft and recipient common iliac artery (black arrow).
reoperations, such as surgical thrombectomy, are mandatory in patients with complete parenchymal necrosis. However, in the absence of graft necrosis, surgery often fails to obtain graft salvage [41]. Moreover, they require general anesthesia and expose to high postoperative morbidity and mortality rates [42]. Systemic anticoagulation therapy is often sufficient in partial venous graft, preventing the propagation of the thrombus, but may be ineffective for extensive luminal obstruction [43]. Endovascular interventions may have a role
in the treatment of these venous thromboses in the absence of parenchymal necrosis [4—8]. They include transarterial thrombolysis, mechanical thrombectomy, thrombus angioplasty or catheter-directed-thrombolysis with aspiration thrombectomy. A successful transarterial thrombolysis was reported by Yoshimatsu et al. but this technique results in a delayed recanalization and requires high doses of urokinase [4]. Mechanical thrombectomy and thrombus angioplasty using an inflated-balloon catheter has been described in one
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Figure 3. 34-year-old woman with graft venous thrombosis 19 days after simultaneous pancreas—kidney transplantation: a: contrastenhanced computed tomography image in the coronal plane shows a defect within the pancreatic graft portal vein (arrow) and pancreatic edema (star); b: initial pancreatic graft portal venography performed via a right femoral vein approach, confirms presence of proximal thrombosis (arrow); c: fluoroscopy image shows thrombus angioplasty using a 10-mm diameter inflated-balloon catheter; d: final pancreatic graft portal venography shows significant restoration of venous outflow.
patient by Izaki et al., allowing graft salvage, but carries the risk of venous anastomosis injury (Fig. 3) [5]. Percutaneous endovenous thrombolysis with aspiration thrombectomy is the most reported technique [6—8,35]. Barrufet et al. have evaluated 17 patients, and reported patient and pancreas graft survival rates at 12 months of 94 and 76%, respectively, without any procedure-related complication [7]. By comparison, a graft salvage rate of 45% was reported by Fridell et al. using surgical thrombectomy [42]. Usually through a venous femoral access, the splenic and mesenteric veins are directly catheterized, preferably with a dedicated hydrodynamic mechanical thrombectomy device. The thrombus can then be removed, with or without prior injection of a chemical thrombolytic therapy. Immediate restoration of venous flow is confirmed by a final venography (Fig. 4). Some authors have also reported the use of metallic stents for residual thrombus or anastomotic kinking or stenosis [35]. Arterial thrombosis is less frequent than venous thrombosis but their actual incidence is not well known. Arterial thrombosis conveys a poor prognosis. Some authors have attempted to treat arterial thrombosis by catheterdirected-thrombolysis, with discouraging results, probably due to the small size of pancreatic vessels [8].
Arterial stenosis Arterial stenosis has a reported incidence of 2.5%, commonly occurs during the early postoperative period and usually at anastomotic sites [33,44]. Ultrasound Doppler findings include increased velocities and turbulent flow at the anastomotic site. The diagnosis can be confirmed with CT. Investigation of vascular stenosis is possible using MRI but may be affected by surgical clips related to transplantation surgery [33]. Arterial stenosis may lead to pancreatic ischemia, in particular in patients with a low iliac inflow because of an underlying atherosclerotic disease. Percutaneous transluminal angioplasty seems to be a suitable therapeutic option for persistent stenosis with hemodynamic consequences [8—10]. The benefits of stent placement in these situations is difficult to evaluate clinically due to limited literature data but should be discussed by analogy with transplant renal artery stenosis [43].
Pseudoaneurysm and arterio-enteric fistulae Hemorrhagic complications are among the most lifethreatening complications following pancreas transplantation. With an estimated prevalence of 2.4% [45], they
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Figure 4. 53-year-old man with graft venous thrombosis 3 days after solitary pancreas transplantation: a: contrast-enhanced computed tomography image in the coronal plane shows a sub-occlusive thrombus within the pancreatic graft portal vein, involving splenic and superior mesenteric veins and extending to the inferior vena cava (arrow); b: initial pancreatic graft portal venography via a right femoral approach, confirms the presence of a nearly occlusive thrombus (arrow); c: transcatheter thrombolysis was performed using urokinase injected through a 5-F pigtail catheter, associated with aspiration thrombectomy through a 7-Fr guiding sheath. Final pancreatic graft portal venography shows a marked restauration of portal flow; d: follow-up contrast-enhanced computed tomography image I the coronal plane obtained 2 months after thrombolysis shows a nearly fully patent portal vein (arrow) with normal parenchymal enhancement of pancreatic transplant.
include pseudoaneurysms and arterio-enteric fistulae. As for bleeding in patients with native pancreas, interventional radiology plays a role in the management of these complications [46]. Pseudoaneurysms most commonly occur at transplant splenic and superior mesenteric artery anastomoses [47]. They may result from surgical technique, biopsy, infection or pancreatitis [33,48]. Transplant pancreatic artery pseudoaneurysm are often asymptomatic, but can also cause graft dysfunction or potentially lifethreatening hemorrhage [48,49]. On Doppler ultrasound, a pseudoaneurysm presents as an anechoic structure, with a characteristic bidirectional internal flow (i.e., the so-called ‘‘yin-yang’’ appearance). Cross-sectional imaging shows pseudoaneurysms as saccular lesions arising from the injured vessel, enhancing similarly to other arteries after injection of contrast material. Treatment of pseudoaneurysms is necessary because of the risk of graft dysfunction or life-threatening bleeding [50,51]. An endovascular approach is suitable for hemodynamically stable patients, including transcatheter embolization and/or covered stent placement. Embolization may be performed with various embolic materials, such as coils, plugs, detachable balloons or glue [8,11], but exposes to allograft or bowel necrosis in these end arteries. Stent-graft placement must be considered for pseudoaneurysms arising from larger arteries, typically iliac
vessels involved in the anastomosis (Fig. 5) [13]. Results from the literature, mainly based on case reports and small studies, suggests that endovascular management of pseudoaneurysms is usually feasible with rare losses of graft function but a relatively high complication rate (33.3%) [12—14]. In infected pseudoaneurysms arising from iliac vessels, stent grafting may still be considered, with low incidence of stent infection [15], but surgical resection of the aneurysm is often required for associated peripancreatic abscess. Rupture of a pseudoaneurysm in the duodenum C-loop used for enteric drainage of pancreas transplants is known as arterio-enteric fistula. This is a rare but life-threatening condition, due to the risk of major gastrointestinal bleeding. As for pseudoaneurysms, interventional radiology can play a role in the management of arterioenteric fistula, especially for patients at high surgical risk. Endovascular exclusion of the fistula may be performed using transcatheter embolization with coils, particles or glue, or using covered stenting of the involved artery [12,16,17].
AVF AVF is a rare complication of pancreas transplantation, with an estimated incidence of 1.4% [52]. AVF may result
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Figure 5. 36-year-old woman with hemorrhagic shock and arterial pseudoaneurysm 10 days after pancreas graft explantation: a: contrastenhanced abdominal computed tomography image with maximal intensity projection in the coronal plane shows large pseudoaneurysm (arrow) arising at site of previous end-to-side anastomosis; b: initial digital subtraction angiogram via a right femoral approach confirms the presence of a pseudoaneurysm (star) arising at site of previous end-to-side anastomosis (arrow); c: endovascular treatment was performed by placing 13.5 × 40 mm iliac covered stent-graft (Fluency® , Bard). Final angiogram shows complete exclusion of the pseudoaneurysm by the covered stent (between arrowheads).
Figure 6. 42-year-old man presenting with an asymptomatic arteriovenous fistula 2 months after simultaneous pancreas—kidney transplantation: a: color Doppler ultrasound shows pulsatile arterialized flow in the draining vein, suggesting pancreas graft arteriovenous fistula; b: contrast-enhanced computed tomography image in the coronal plane during the arterial phase shows early opacification of the portal vein (PV) through an arteriovenous fistula (arrow) fed by the pancreas graft superior mesenteric artery (SMA); c: initial digital subtraction angiogram of pancreatic graft via a right femoral approach shows early venous drainage (arrow) confirming the presence of a large arteriovenous fistula (PV: portal vein; SMA: superior mesenteric artery); d: angiogram shows superior mesenteric arterial feeder supplying the arteriovenous fistula that was embolized using a 10-mm Amplatzer® vascular plug (AGA Medical Corp.) (between arrowheads). Postembolization angiography confirms occlusion of arteriovenous fistula and no further opacification of the early draining vein.
from the postoperative (blind ligation or surgical stapler) or post-biopsy laceration of both arterial and venous walls. AVF can be seen either on transplant mesenteric root (superior mesenteric vessels) or on pancreatic tail (splenic vessels). Persistent AVF may potentially lead to major bleeding or graft loss if untreated [53,54]. Doppler ultrasound shows focal aliasing with a high velocity, low-resistance
arterial inflow and a pulsatile arterialized draining vein [54]. Cross-sectional imaging may show enlarged Y-graft arteries with an early opacification of the donor draining vein during arterial phase [48]. Transcatheter angiography remains the gold standard for the diagnosis of AVF, showing dynamic images and allowing for endovascular treatment [18]. Persistent and/or symptomatic large AVF
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Figure 7. 45-year-old man peripancreatic fluid collection 9 days after simultaneous pancreas—kidney transplantation: a: contrastenhanced abdominal computed tomography image in the axial plane shows well-defined fluid collection (star) around the pancreas transplant with peripheral rim enhancement (arrowheads); b: percutaneous drainage was performed using a 12-Fr drainage catheter (Cook) inserted under computed tomography guidance through an anterior approach. Due to the presence of Candida albicans in the fluid content, fluconazole was given during 6 weeks with a daily dose of 400 mg. The catheter was removed 1 month later; c: follow-up computed tomography image in the axial plane obtained 4 months later shows no residual fluid collection.
Figure 8. 53-year-old man with suspected graft rejection 14 days after solitary pancreas transplantation: a: contrast-enhanced abdominal computed tomography image in the axial plane shows mild enlargement of pancreas transplant (star) with slightly heterogenous enhancement; b: percutaneous biopsy was performed under real-time ultrasound guidance, using an 18-Gauge biopsy needle (arrow) advanced into the pancreas transplant (star). Histopathologic analysis of tissue sample confirmed acute cellular rejection.
must be treated, either by surgical or endovascular approach [19,53]. However, surgical ligation of pancreatic transplants AVF has been abandoned progressively, in favor of much less invasive transcatheter embolization [19]. Large occlusive materials, including coils, detachable balloons and plugs, should be used, as liquid embolic agents may result in allograft ischemia and/or nontarget embolization (Fig. 6) [19—23].
Extravascular complications Peripancreatic fluid collections The development of fluid collections adjacent to pancreas transplants has an estimated incidence of 11% to 16% [55,56]. Their presence is associated with a lower pancreas graft survival rate and a greater incidence of infection by comparison with patients without fluid collection (68% and 75% vs. 85% and 46%, respectively) [55]. Fluid collections may complicate intestinal leakage, pancreatitis, open lymphatics, hemorrhage or infection. They can be encountered in the early or late postoperative course following transplantation. Collections appear hypoechoic on ultrasound, except for hematomas and some abscesses that may contain
internal echoes [33]. CT shows hypo-attenuating welldefined lesions, while hematomas have hyper-attenuating content. A peripheral rim enhancement may be seen in abscesses or superinfected collections [55]. MRI may help identify hemorrhagic content because fresh blood displays hypersignal on T1-weighted images [57]. In particular, patients for whom differentiation between graft pancreatitis and leakage from the anastomosis is difficult, the use of secretin-stimulated MRI may be valuable by showing active pancreatic fistula filling the collection [58]. Percutaneous ultrasound or CT-guided needle-aspiration may be useful for further biochemical and bacteriological analysis. Up to 80% of fluid collections can be managed conservatively with percutaneous drainage [24]. Reintervention is only needed for anastomotic leakage in patients with enteric drainage, failure of conservative treatment or for hemodynamically unstable patients [24]. Percutaneous drainage can be performed either under ultrasound or CT guidance, depending on the location of the collection and operator’s preference (Fig. 7). There is no consensus regarding the size of the drainage catheter or the duration of drainage in this indication. In our experience, we routinely use 8- to 14-Fr caliber catheter, depending on the nature of the fluid, and a drainage duration of 7 to 10 days is usually sufficient before catheter removal.
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Graft rejection Despite the continuous advances in the field of immunosuppressive therapies, pancreas transplant rejection remains the first cause of graft loss after one year, with rates varying between 5% and 25% [59]. Rejection may occur immediately (hyperacute), 1 week to 3 months post-transplant (acute) or after months post-transplant (chronic). Imaging findings of rejection are non-specific, the main differential diagnosis being graft pancreatitis. At ultrasound, acute rejection presents as graft enlargement and increased parenchymal heterogeneity. Duplex and color Doppler ultrasound are also useful to exclude thrombosis. CT may show gland enlargement with heterogenous enhancement and occasionally peripancreatic fluid collections [33]. On MRI, in patients with acute rejection, pancreatic graft is hyperintense on T2weighted images due to parenchymal edema and pancreas enhancement is often altered as on CT. Chronic rejection usually results in atrophy of pancreatic graft and MRI may show decreased signal of the pancreas transplant on T1- and T2-weighted images [60]. Although rejection may be suspected on ultrasound, CT or MRI, final diagnosis and grading of both acute and chronic rejection require histopathological analysis [61]. The most common method for obtaining tissue sample is percutaneous biopsy using 18-Gauge automatic biopsy needles [25]. Ultrasound is often sufficient for guidance, offering radiation-free and real-time monitoring (Fig. 8) [25]. CT guidance may be necessary when bowel gas interposition obscures the anterior approach. According to Atwell et al., adequate allograft pancreatic tissue can be obtained with percutaneous needle biopsy in more than 96% of procedures, with less than 3% of biopsies resulting in major complications [25].
Conclusion Pancreas transplantation is a complex surgical intervention, exposing vulnerable patients to a large variety of vascular and nonvascular complications. Interventional radiologists should be familiar with pancreas transplant anatomy and surgical techniques in order to play a key role in the diagnosis and management of these complications, potentially improving outcomes for patients.
Disclosure of interest
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The authors declare that they have no competing interest.
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