Current Opinion in Organ Transplantation:
PANCREAS TRANSPLANTATION: Edited by Walter mark
Risk factors for and management of graft pancreatitis
Nadalin, Silvio; Girotti, Paolo; Königsrainer, Alfred
Department of General, Visceral and Transplant Surgery, Tuebingen University Hospital, Germany
Correspondence to Silvio Nadalin, MD, FEBS, Department of General, Visceral and Transplant Surgery, Tuebingen University Hospital, Hoppe Seyler Str 3, 72076 Tübingen, Germany. Tel: +49 7071 2986600; fax: +49 7071 294934; e-mail: email@example.com
Purpose of review: Systematic and detailed analysis of risk factors, pathophysiology, clinical manifestation, diagnosis and management of graft pancreatitis in its different forms, that is acute and chronic graft pancreatitis (A-GP and C-GP), and A-GP being further distinguished into: physiological (P-AGP), early (E-AGP) and late AP (L-AGP).
Recent findings: Graft pancreatitis is the second most-frequent complication following pancreas transplantation. P-AGP is an unavoidable entity related to ischemic reperfusion injury. It is usually clinically silent. It is a timely and prognostically self-limited process. E-AGP occurs within 3 months after pancreas transplantation (PTx) in 35% of cases and is associated with high rates of graft loss (78–91%). Clinical signs are pain, systemic inflammatory response (SIRS) and haematuria. Therapy can be medical, interventional and surgical. L-AGP occurs 3 months following PTx in 14–25% of cases and represents an uncommon cause of graft loss. Typical clinical signs are pain, abdominal tenderness and fever. Typical laboratory signs are hyperamylasaemia, hyperglycaemia and hypercreatininaemia. Therapy is usually conservative. C-GP is difficult to be distinguished from chronic rejection and is associated to graft loss in 4–10% of cases. Recurrent A-GPs and infections are the main risk factors. Specific symptoms are chronic abdominal malaise, constipation and recurrence of DM. Isolated hyperglycaemia is typical of C-GP. The therapy is usually conservative.
Summary: This systematic analysis of different manifestations of graft pancreatitis provides the basis for a clinical approach to tackling this complex entity.
After vascular thrombosis, graft pancreatitis is the second most-frequent complication following pancreas transplantation in its various techniques.
To date there is no standard definition for graft pancreatitis. Most definitions conform with the ones usually used for classical acute and chronic pancreatitis.
For didactic reasons two major entities of graft pancreatitis are distinguished: acute and chronic graft pancreatitis (A-GP and C-GP). A-GP has been further distinguished in three subtypes: physiological (P-AGP), early (E-AGP) and late A-GP (L-AGP).
We here describe the above-mentioned different forms of graft pancreatitis in detail.
PHYSIOLOGICAL ACUTE GRAFT PANCREATITIS
Physiological acute graft pancreatitis occurs in 100% of pancreas transplantation (PTx) secondarily to an acute inflammatory response related to ischaemic reperfusion injury (IRI). It may occur between 30 min and 72 h after reperfusion.
Per se there is not a single particular risk factor for P-AGP apart from IRI, which is intrinsically related to the procedure itself. Moreover, various factors like cold ischaemia time (CIT), donor age and microvascular disease of the graft may influence P-AGP entity [1–3].
The pathophysiological mechanism of P-AGP was recently described in detail by Busing et al.. Induced by ischaemia (hypoxia) and reperfusion-related damage to the graft, capillary endothelial cells undergo a displacement of energy involving acidosis and the production of oxygen-free radicals (usually within the endoplasmic reticulum). This causes necrosis of endothelial cells with consequent endotheliitis and arteritis, thus leading to microvascular thrombosis and an increase in hypoxic damage and consequently in lymphocytic infiltration. This has been reported in the context of acinar necrosis and may trigger an immunological reaction (so-called innate immunity).
As a pancreas graft biopsy is usually not performed immediately after reperfusion or at the end of the operation, the pathological findings of P-AGP have been derived from animal studies, in which the following pathological patterns were described :
3. Granulocytic infiltration
Although P-AGP appears clinically silent, it is usually associated with high levels of amylase or lipase in drain fluids and systemically increased C-reactive protein (CRP).
Complications and prognosis
Due to its nature and perioperative administration of steroids and anticoagulant medication acting at different inflammatory phases, P-AGP is a timely and prognostically limited process.
Apart from histological patterns associated with P-AGP, no reports on diagnostic procedures have been available in the literature concerning this particular form of graft pancreatitis.
Therapy and prophylaxis
As P-AGP is an unavoidable entity, the only possibility is to limit this acute inflammatory process at different stages of pancreas transplantation :
1. The pancreas is already at risk for severe oedema upon brain death when the donor undergoes aggressive fluid resuscitation and later after revascularization upon reperfusion in the recipient. In this context, steroids administered along the retrieval procedure as well as the recipient operation may counteract the damage.
2. Calcium channel blockers may improve organ function by inducing better perfusion and reducing a high intracellular calcium concentration, which usually leads to cell death after IRI.
3. Hypotension, hypovolaemia and high doses of catecholamines at reperfusion (here, anaesthesiological management plays a pivotal role) should be avoided.
EARLY ACUTE GRAFT PANCREATITIS
Occurring with an incidence of 35–38% mainly within 3 months after PTx, E-AGP is an acute form of pancreatitis. It develops either spontaneously or as a consequence of surgical complications [4▪▪,5–7].
1. Donor [4▪▪,7,8,9▪]:
a. age above 50
b. cardio-cerebro-vascular cause of death
c. significant haemodynamic instability
d. massive volume resuscitation
2. Graft procurement :
a. Procurement technique [4▪▪,7] not in accordance with the standard guidelines and the technical pitfalls reported in the literature . that is:
i. careful ‘no-touch’ technique [12,13]
ii. identification of and respect for the inferior pancreaticoduodenal artery 
iii. ’en-bloc’ multivisceral procurement and ex-situ preparation of pancreas graft with consequent reduction of in-situ warm ischemia and careful preparation of vascular structures [10,15,16].
b. The procurement surgeon plays a key role in this context. In fact, as recently reported by Stratta et al., there is no difference in transplant outcome between local and imported pancreas allografts when the graft is retrieved by an experienced PTx surgeon.
c. Preservation solution: the literature contains controversial data on preservation solutions . Various authors reported a higher incidence of allograft pancreatitis and graft loss in cases of pancreata flushed with histidine-tryptophan-ketoglutarate (HTK) as compared with University of Wisconsin solution [19–21]Conversely, a recent randomized, controlled study failed to show any significant difference between HTK and University of Wisconsin solution for pancreas allograft preservation . Similar results have been reported by Fridell et al.[23,24] and Becker et al..
d. The back table phase: preparation of the pancreas graft at the back table requires good surgical skills and should therefore be performed by an experienced pancreas transplant surgeon. Additionally, particular technical pitfalls such as meticulous reconstruction of the superior mesenteric and splenic arterial inflow, avoidance of extension grafts of the portal vein or even revascularization of the gastroduodenal artery and the right gastroepiploic vein [4▪▪,26] require the surgeon's cautious attention [27–30].
3. Recipient operation
a. Endocrine drainage: portal versus systemic. Although theoretically, portal drainage is more physiological and should improve postoperative control of glucose metabolism , several studies have definitively demonstrated that portal vein drainage is at least equivalent to systemic drainage with regard to patient and short-term graft survival rates and technical complication rates [32,33]. For this reason, most PTx centres have abandoned portal vein drainage because of technical difficulties and increased morbidity as a result of venous thrombosis and enteric leaks .
b. Exocrine drainage.Stratta et al. reported a slight increase in E-AGP in patients with exocrine drainage into the bladder (see also pathophysiology).For patients with intestinal drainage Grochowiecki et al. considered the fact that the postoperative swelling of the papilla Vateri may create an obstacle to pancreatic juice outflow with consequent oedema of the pancreas graft and graft pancreatitis. The authors thus suggest that an open sphincterectomy should be performed to decompress the pancreatic graft .
4. RecipientRecipients who underwent peritoneal dialysis prior to transplantation  and those with hypercoagulability status  showed a higher frequency of E-AGP.
5. Infection [4▪▪,26,37]
a. Cytomegalovirus (CMV)Due to the current prophylaxis policy, CMV infection is rarely associated with acute graft loss as the result of early acute graft pancreatitis [38–40].
b. Fungal infectionCandida (albicans and glabrata) and other fungal infections are infrequent, but possible agents of acute necrotizing pancreatitis. Consequently, proper antifungal prophylaxis is essential .
An immunosuppressive regimen with cyclosporin A may increase the risk for E-AGP [42–45].
With regard to pathophysiology, two different kinds of E-AGP are distinguished.
1. E-AGP pure
a. postinfective (i.e. CMV and fungal) 10%
b. immunological (i.e. acute rejection) 30%
2. E-AGP related to surgical procedure:
a. Vascular thrombosisVascular thrombosis is responsible for 60–70% of E-AGP cases and is secondary to technical problems in 59% of patients with E-AGP or can be associated with immunological endothelial damage (e.g. hyperacute rejection) in 33% of cases 
b. Exocrine bladder drainageReflux of bladder-duodenal content with active trypsin and infected urine may damage the ductal mucosal barrier, resulting in intrapancreatic activation of enzymes [47–49].
Typical signs of post-thrombotic pancreatitis are focal or diffuse ischaemic (coagulative) or haemorrhagic necrosis .
Fibrinoid necrosis of arteries and veins associated with massive vascular thrombosis and parenchymal necrosis (IgG and C3 positive in the wall of blood vessels) has been shown to be typical of E-AGP secondary to hyperacute allograft rejection [50,51].
Endotheliitis and various degrees of necrotizing arteritis are the typical histological signs (acute rejection grades IV and V) of acute allograft rejection [50,51].
Typical clinical signs of E-AGP are pain (due to graft tenderness and enlargement), systemic inflammatory response (SIRS) (in the case of complications) and haematuria (in the case of exocrine bladder drainage) [4▪▪,6,7].
Complications and prognosis
Early acute graft pancreatitis is associated with 1-year graft loss rates of 78–91% and with suprainfection rates with consequent SIRS in 10–20% of cases [4▪▪,7,52].
b. Hyperamylasemia (not present in case of rejection alone)
a. Sonography can detect heterogeneous parenchymal echotexture, pancreatic duct dilatation and change in blood flow, but cannot assess vessel contour abnormality. Sonography is thus not a reliable means of identifying acute organ rejection or pancreatitis and, moreover, is operator-dependent .
b. Computed tomography (CT) scan is the gold standard for the diagnosis of complications following PTx. It is widely available and relatively low in cost. Moreover, rapid image acquisition multidetector CT (MDCT) is a quick noninvasive means of identifying the cause of pancreatic graft dysfunction when renal function is not markedly impaired. CT scan is useful for demonstrating the extent and severity of graft pancreatitis. CT findings are similar to those for native pancreatitis, that is peripancreatic fat stranding and peripancreatic collections [53–56]. Additionally, a CT-guided biopsy of the graft can also be performed.
c. Contrast-enhanced magnetic resonance (MR) angiography has been shown to reliably assess the vascular anatomy in cases of impaired graft function or suspected vascular complications. However, the following two possible complications should be kept in mind: the risk for nephrogenic systemic fibrosis from gadolinium administration in the setting of severe renal impairment and the possible induction of movement of surgical clips during the early postoperative period [57,58].
1. Medical (depending on cause) [4▪▪,7].
a. Antithrombotic therapy
b. Bowel rest and temporary administration of total parenteral nutrition
c. Treatment of concurrent infections
2. Radiological interventionalIn the case of vascular thrombosis transarterial or transvenous graft salvage procedures with long-term graft survival rates of 50% have been reported [59–61].
3. SurgicalTo date the literature contains no clear standardized guidelines for timing or type of surgical procedure like necrosectomy or graft explantation. These procedures depend on intraoperative findings, clinical course and the surgeon's experience. If a pancreas graft is removed, a pancreas re-transplantation should not be performed before 2–4 weeks [5,8,62–64].
LATE ACUTE GRAFT PANCREATITIS
Graft pancreatitis occurring 3 months following PTx may be termed L-AGP and has been observed in 14–25% of cases [65,66].
Risk factors and pathophysiology [38,66]
1. Exocrine bladder drainage: most cases of L-AGP are attributed to urinary reflux, urinary tract infection or bladder outflow obstruction. In this last case a bladder pressure above 20 cmH2O2 may induce a vascular disorder such as a decrease in differential venous pressure, resulting in acute ischaemia.
2. Mechanical stricture and trauma or direct mechanical pressure to the graft.
3. Direct traumatic injury of the graft.
4. Intraparenchymal microvascular thrombosis due to a chronic immunological disturbance that does not induce acute rejection, but may chronically influence venous outflow from the pancreas graft and consequently cause ischemic damage.
5. Recurrent infection surrounding the graft like in the case of a late microleak of exocrine drainage.
6. Occlusion of Oddi's sphincter secondary to rejection.
7. CMV infection: as reported above, CMV infection is rarely associated with acute graft loss due to the development of early acute graft pancreatitis, but CMV reactivation seems to be associated with delayed graft function and the risk for late acute pancreatitis and chronic recurrence of diabetes mellitus (DM) [38,40].
Typical signs of L-AGP are lymphocytic infiltrates involving the pancreatic duct and its branches. It should be differentiated from acute late rejection, which presents with the pathognomonic vascular changes of endothelialitis or vasculitis [46,50]
The most frequently reported symptoms of L-AGP are pain in 100%, abdominal tenderness in 87% and fever in 64% of cases. In 48% of cases associated symptoms are also reported: vomiting, diarrhoea and bloating [47,66–71].
Rare manifestations of L-AGP are:
1. acute urinary retention ,
2. erythema nodosum in the pretibial areas (pancreatic panniculitis) [68,72],
3. haemorrhagic cystitis in patients with bladder drainage .
Late acute graft pancreatitis is an uncommon cause of graft loss.
In patients with L-AGP overall graft survival at 1, 3 and 5 years has been reported to be 95, 93 and 89%, respectively [66,73].
1. LaboratoryThe typical laboratory sign of L-AGP is the triad hyperamylasemia + hyperglycaemia + hypercreatininaemia or an increase of inflammatory parameters.Graft pancreatitis can be differentiated from acute rejection on the basis of marked hyperamylasemia and significant local findings adjacent to the allograft, both of which are not characteristic of acute rejection (usually characterized by isolated hyperglycaemia) [66,74,75].It is important to mention that in patients with bladder drainage urinary amylase does not correlate with L-AGP .
a. Sonography: detection of peripancreatic fluid collections and presence or absence of blood flow .
b. Computed tomography: this is the gold standard radiological investigation for diagnosis of L-AGP. It demonstrates pancreatic infiltration, oedema, and peripancreatic fluid [47,66,71].
Most authors [47,66–71] who have reported on L-AGP suggest the following therapeutic principles:
1. Bowel rest (100%)
2. Hydration (100%)
3. Close monitoring (100%)
4. Antibiotics (50–73%)
In patients with complicated L-AGP a percutaneous or operative drainage is suggested in 12% and relaparotomy without pancreatectomy in 12%.
In case of L-AGP associated to complicated course after bladder drainage, the enteric conversion of the exocrine drainage may result in excellent long-term graft function and significant resolution of symptoms even years after SPK. Notwithstanding, postoperative morbidity after enteric conversion including early reoperation and graft loss has to be considered . No clear data about indication and timing of pancreatectomy have been reported.
CHRONIC GRAFT PANCREATITIS
No clear definition of chronic graft pancreatitis (C-GP) has been established to date because its nature is characteristically an overlapping of chronic rejection and chronic pancreatitis. Similarly, no data have been reported on its incidence [46,50,51]
Risk factors and pathophysiology
The literature also contains very few data on these two aspects. The main pathogenic factors can be considered to be:
1. Inflammatory: recurrent acute pancreatitis of different cause
2. Immunological: chronic rejection
3. Infective: CMV and fungal
Typical histological features of C-GP are isleitis (i.e. disruption of beta cells), extensive interstitial fibrosis, acinar atrophy and obliterative arthritis .
Specific symptoms of C-GP are [46,50,51]:
1. Chronic abdominal malaise
2. Chronic obstipation
3. Recurrence of DM
Chronic graft pancreatitis can be complicated by suprainfections.
It is a cause of late graft loss in 4–10% of cases [46,50,51].
1. LaboratoryThe typical sign of C-GP is isolated hyperglycaemia with no changes in amylasemia.
2. ImagingComputed tomography and MRI usually show a retracted fibrotic graft.
No clear data/guidelines have been established to date.
In patients with C-GP but without complications we suggest a conservative therapy. A graft pancreatectomy should be performed for local and systemic complications and to halt immunosuppression in cases of pancreas transplantation alone.
In this study we have reviewed the concept of graft pancreatitis in its different forms, i.e. physiological, early acute, late acute and chronic graft pancreatitis.
This systematic analysis of different manifestations of graft pancreatitis provides better understanding and therefore the basis for a clinical approach to tackling this complex entity.
We would like to express our immense gratitude to Ms Mary Margreiter for her essential support in improving the English grammar and syntax of the text.
Conflicts of interest
There are no conflicts of interest to declare.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
▪ of special interest
▪▪ of outstanding interest
Additional references related to this topic can also be found in the Current World Literature section in this issue (pp. 124–125).
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complications; graft pancreatitis; pancreas transplantation
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