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A retrospective monocenter review of simultaneous pancreas-kidney transplantation
with bladder drainage in China
BI Hai, HOU Xiao-fei, MA Lu-lin, LUO Kang-ping, WANG Guo-liang, ZHAO Lei and LIU Ya-li
Department of Urology, Third Hospital of Peking University, 49 North Garden Road, Haidian District,
Beijing 100191, China.
Correspondence to: HOU Xiao-fei
Department of Urology, Third Hospital of Peking University,
49 North Garden Road, Haidian, Beijing 100191, China
Email: [email protected]. Tel: +86-10-82267521. Fax: +86-10-82020576.
Keywords: pancreas transplantation; kidney transplantation; survival rate; postoperative complications
ABSTRACT
Background Simultaneous pancreas-kidney transplantation (SPKT) frees the diabetic patient with
end-stage nephropathy from dialysis and daily insulin injections. Herein, we review consecutive cases of
SPKT with bladder drainage performed at our institution over an 8-year period.
Methods The study population included 21 patients (16 males and 5 females) who underwent SPKT
between September 2001 and September 2009. Seven patients had type-1 diabetes and 14 had type-2
diabetes. Nineteen patients were on dialysis at the time of transplantation. Donation after cardiac death
donors were selected for SPKT. The mean human leukocyte antigen match was 2 (range=0–4). SPKT was
always performed using bladder drainage and vascular anastomoses to the systemic circulation.
Immunosuppressive treatment consisted of anti-lymphocyte globulin induction followed by tacrolimus,
mycophenolate mofetil, and prednisone.
Results The mean hospital stay was 45.43 days. After a mean follow-up of 39.4 months, survival rates for
patient, kidney, and pancreas were 76.2%, 76.2%, and 66.7% at 1 year; 76.2%, 59.3%, and 55.6% at 5
years; and 57.1%, 39.5%, and 41.7% at 8 years, respectively. Major complications included anastomotic
leaks, reflux pancreatitis, and rejection. Six patients died from septic shock (n=3), duodenal stump leak
(n=1), cardiac arrest (n=1), or renal failure (n=1). Eight kidney grafts were lost due to acute rejection
(n=2), chronic rejection (n=3), and death with a functioning graft (n=3). Pancreatic graft failure (n=9) was
caused by thrombosis (n=1), rejection (n=2), duodenal stump leak (n=1), and death with a functioning
graft (n=5).
Conclusions Few hospitals in China can undertake SPKT because patients must pay their own expenses
and the postoperative management and complications can be difficult. However, SPKT is a valid
therapeutic option for uremic diabetics. For this reason, we want to share our experiences with our
colleagues to promote the development of SPKT in our country.
INTRODUCTION
The first simultaneous pancreas-kidney transplant (SPKT) was performed by Kelly et al more than 40
years ago at the University of Minnesota.1 After decades of controversy surrounding the therapeutic
validity of pancreatic transplantation, SPKT is now a procedure that frees the diabetic patient with
end-stage nephropathy from dialysis and daily insulin injections. With advancements in surgical
technique, immunosuppressive regimens, and immunological testing, the success rate of SPKT has
improved in the current era.2 Here, we review a consecutive series of SPKT with bladder drainage
performed at our institution over an 8-year period in China.
METHODS
Study population
Between September 2001 and September 2009, 21 patients (16 males and 5 females) underwent SPKT at
our center. The mean recipient age was 44.05 years (range=26–59 years). Seven patients had type-1
diabetes mellitus and 14 had type 2 diabetes mellitus. All were primary transplants. Nineteen patients
were on hemodialysis at the time of transplantation and two underwent peritoneal dialysis before
hemodialysis.
Of the 21 patients described in this study, all were diagnosed with insulin-dependent diabetes. The
mean duration illness was 14.52 years (range=8–20 years). Apart from end-stage nephropathy, they also
had other manifestations of diabetes, including retinopathy (n=14), neuropathy (n=5), dermatopathy (n=3),
and cardiopathy (n=2). Patients with a history of cardiac interventions were eliminated from our program.
We selected donation after cardiac death (DCD) donors for SPKT. The mean warm ischemic time for
the pancreas and kidney grafts was 5.21 minutes (range=3–9 minutes) and the mean cold ischemic time
was 7.37 hours (range=2–16 hours) and 7.18 hours (range=2–16 hours), respectively. The recipients were
selected for transplantation on the basis of blood group compatibility, a negative cross match and a
negative panel reactive antibody (PRA); except for two cases (PRA of 55% and 35%). The mean human
leukocyte antigen (HLA) match was 2 (range=0–4).
Surgical procedures
Donor operative procedure
The procurement procedure began with a long midline incision extending from the xiphoid process
to the pubic symphysis. We dissociated the abdominal aorta in the retroperitoneal cavity and a self-made
Foley infusion catheter (F20–22) was inserted 15 cm into the aorta 4–5 cm above the bifurcation of the
common iliac artery. University of Wisconsin (UW) solution (3000 ml) was infused into the aorta, while a
drainage catheter was inserted into the inferior vena cava at the same time to keep the operation field clear.
The kidneys and ureters were then dissociated. The duodenum was cut off at its juncture with the stomach
and jejunum. Mobilization of the pancreas was begun by incising the posterior and lateral peritoneal
attachments of the spleen. The spleen was then grasped and the dissection was continued posteriorly in a
lateral-to-medial direction. The spleen was procured in continuity with the tail of the pancreas. The
anterior side of pancreas was dissociated close to the stomach and we cut off the jejunum below Treitz’s
ligament. Next, the portal vein was cut off below the porta hepatis to keep the portal vein as long as
possible. The kidneys, duodenum, pancreas, and spleen were then removed en bloc, placed in a plastic
bag, and cold-stored in UW solution at 4°C.
Trimming of the pancreas and kidney
First, we dissociated the portal vein, celiac trunk, and superior mesenteric artery. Then the patch
containing the celiac trunk and superior mesenteric artery was cut from the aorta. The proper hepatic
artery was ligated, with close attention paid to preserving the stomach-duodenal and pancreas-duodenal
arteries. Second, the splenic vessels were ligated so as not to damage the tail of the pancreas. The tissues
above and below the pancreas were ligated twice, especially at the head and body of the pancreas. The
common bile duct was also ligated close to the pancreas. Third, the blood vessels serving the kidneys
were dissociated and excess perirenal fat was removed. The ureters were kept 9–12 cm below the pelvis,
while the fat around the ureters was preserved in case of a reduction in blood supply and to prevent any
urinary leaks.
Recipient operation procedure
In brief, the abdomen was entered through a long midline incision about 20–25cm long and the
bilateral common iliac artery and iliac veins were dissociated. The pancreas was transplanted into the
right iliac fossa, while the portal vein was anastomosed to the external iliac vein and the aortic patch was
anastomosed to the common iliac artery. After flushing the duodenum with physiological saline, the
opposite duodenal side of Vater’s ampulla was anastomosed to the urinary bladder (the diameter of
orificium fistulae is about 2.5 cm) and the two stumps of the duodenum were closed. The length of the
duodenum was 7–10 cm. The kidney was transplanted into the left iliac fossa and the renal vein
anastomosed to the external iliac vein and the renal artery anastomosed to the external iliac artery. The
ureter was anastomosed to the left side of the bladder. A midline closure was accomplished with running
1-0 prolene and interrupted 1-0 Ticron sutures.
Immunosuppressive therapy and other medications
Immunosuppressive treatment consisted of ALG induction followed by tacrolimus, mycophenolate
mofetil, and prednisone. Patients received tacrolimus 0.05–0.15 mg/kg/day and mycophenolate mofetil
20–25 mg/kg/day per os before surgery. A continuous intravenous injection of methylprednisolone (0.5–1
g) was given from the day of the operation to post-operative Day 3. ALG (250 mg/day) was then given
for 7–10 days. On the first day post-surgery, tacrolimus 0.07–0.15 mg/kg/day, mycophenolate mofetil
1–1.5 g/day, and prednisone 20–30 mg/day was used as the initial immunosuppressive treatment. The
blood concentration of tacrolimus was monitored twice a week, and the dose adjusted to maintain a blood
concentration of 15–25 g/l (peak concentration) and 5–15 g/l (trough concentration). Aspirin (100 mg)
was given per os once a day for 14 days to prevent thrombosis of the pancreas. Somatostatin 0.1 mg Q8h
was given via subcutaneous injection for 14 days to prevent pancreatitis. Sodium bicarbonate (5%) was
given daily for 10 days via intravenous injection to prevent metabolic acidosis followed by oral Saleratus
(10–20 g/day). At the same time, glucose, albumin, amino acids, and fat emulsion were employed for
nutritional support.
Statistical analysis
All demographic and baseline variables were described by their characteristics. Continuous variables
were summarized by reporting means and categorical variables were summarized by reporting
percentages. Event rates were estimated using the methods of Kaplan and Meier. All analyses were
performed using SPSS v16.0 (SPSS Inc., Chicago, IL, USA).
RESULTS
The mean hospital stay was 45.43 days (range=5–241 days). After surgery, 16 patients had good
pancreatic function, and insulin therapy was stopped in 15 cases immediately after the operation. Insulin
therapy was stopped in one case after 4 days. The recipients had normal pancreatic function, normal
glucose levels, and normal urine amylase (5,000–25,000 u/l). Fifteen recipients had immediate renal
function, while one recipient had delayed renal function. Five patients died, and two recipients lost the
pancreas after surgery. In all, 16 recipients had normal kidney function and 14 patients had normal
pancreatic function. Insulin therapy and hemodialysis were stopped upon discharge.
Patient survival and causes of death
The overall patient survival rate was 71.4% (15/21) after a mean follow-up of 39.4 months
(range=0.2–105.5 months). Kaplan-Meier analysis showed a mean patient survival of 78.52±9.54 months
(95% confidence interval [CI]=59.82-97.22 months). One-, 5-, and 8-year cumulative patient survival
rates were 76.2%, 76.2%, and 57.1%, respectively. Six patients died during the perioperative period and
the principal causes were septic shock (n=3), duodenal stump leak (n=1), cardiac arrest (n=1), and renal
failure (n=1).
Graft survival and cause of graft loss
The rate of kidney graft survival was 61.9% (13/21) after a mean follow-up of 39.4 months.
Censoring for patient death, the mean kidney graft survival period was 63.46±10.78 months (95%
CI=42.33–84.59 months). Cumulative graft survival rates at 1, 5, and 8 years were 76.2%, 59.3%, and
39.5%, respectively. Eight kidney grafts were lost due to acute rejection (n=2), chronic rejection (n=3),
and death with a functioning graft (n=3).
The pancreas survival rate was 57.1% (12/21), defined by normal glucose metabolism without any
anti-diabetic medications. Censoring for patient death, the mean kidney graft survival period was
68.63±6.11 months (95% CI=56.66–80.61 months). Cumulative graft survival rates at 1, 5, and 8 years
were 66.7%, 55.6%, and 41.7%, respectively. Pancreatic graft (n=9) was caused by thrombosis (n=1),
rejection (n=2), duodenal stump leak (n=1), and death with a functioning graft (n=5).
The overall patient, kidney, and pancreas survival rates are shown the Figure.
1.0
Cum Survival
0.8
Life
0.6
Pancreas
0.4
Kidney
0.2
0.0
0.0
20.0
40.0
60.0
80.0
100.0
120.0
Months Post Transplant
Figure. Overall survival rates of pancreas and kidney grafts s from 21 consecutive simultaneous
pancreas-kidney transplants.
Complications
Major complications included rejection, anastomotic leaks, and reflux pancreatitis (Table).
Table. Complications for SPKT
Complications
N (%)
Rejection
Acute rejection
9 (42.9%)
Chronic rejection
3 (14.3%)
Reflux pancreatitis
3 (14.3%)
Anastomotic leaks
Duodenal stump leak
4 (19.0%)
Urine leakage
2 (9.5%)
Metabolic acidosis
3 (14.3%)
Urologic complication
Urinary tract infection
4 (19.0%)
Urolithiasis
2 (9.5%)
Neurogenic bladder
1 (4.8%)
Cytomegalovirus pneumonia
3 (14.3%)
Wound infection
3 (14.3%)
Vascular complication
Thrombus
1 (4.8%)
Erosive vascular rupture
1 (4.8%)
Vascular anastomotic leak
1 (4.8%)
In our center, rejection was recorded in 11 recipients; nine were acute rejection and three were
chronic rejection. The morbidity of rejection was high and we implemented effective therapeutics to
control graft damage. However, there were three kidneys and two pancreases losing their function for
rejection.
Four patients experienced duodenal stump leakage, and these patients all died after surgery. One
reported abdominal pain within 18 days of the operation, with a fever of about 38°C, rebound tenderness
and muscular tension. His drainage fluid amylase rose to 118,500 U/l, but serum amylase was normal.
Cystography suggested a duodenal stump leak and surgical exploration confirmed this diagnosis. This
recipient died of ascending colon leakage during a second repair operation 6 months later. Until his death,
graft function was good. Two other recipients died from erosive hemorrhage and one died from septic
shock. Three recipients had pancreatitis 2 weeks to 2 months after the operation due to the reflux of urine,
and were all controlled at discharge. Three recipients experienced acidosis and dehydration. Their
principal manifestation was inertia and a serum CO2CP level of 15–19 mmol/l.
DISCUSSION
Recent developments in surgical and immunosuppressive techniques have allowed pancreas
transplantation to become an effective treatment to halt the progression of diabetes in selected
individuals.2 According to the International Pancreas Transplant Registry (IPTR),3 large-volume pancreas
centers perform better and have better outcomes. The overall results of this study confirm the validity of
SPKT for the treatment of diabetes complicated by terminal renal failure.
The outcome for SPKT is worse than that for kidney and liver transplantation because there are few
centers that do this kind of surgery. Also, this type of surgery carries a high level of risk due to
complications and patients have to pay their own expenses. We observed patient, kidney, and pancreas
survival rates of 76.2%, 76.2%, and 66.7% at 1 year; 76.2%, 59.3%, and 55.6% at 5 years; and 57.1%,
39.5%, and 41.7% at 8 years, respectively (Figure). Patient and graft survival were comparable with those
reported by Arjona et al.4 They analyzed 101 SPKT performed between 1989 and 2007. After 1, 5, and 10
years, patient survival was 93%, 87.2%, and 91%; pancreas survival was 86%, 79.6%, and 87.8%; and
kidney graft survival was 70%, 70%, and 85%, respectively. We considered our longer term survival rates
to be a little inferior to those presented by other, larger studies.5, 6 The main reason may be a lack of
experience in terms of surgical procedures and perioperative management during the early stages of our
SPKT program. As a result, three patients died within 1 month of surgery, and one patient within six
months. However, the death rate in our center fell as we gained more experience.
Cardiovascular morbidity is an important contributor to overall patient outcomes.5 One of our
recipients had a successful SPKT operation, with no blood infused during the operation. However, he died
on Day 2 post-surgery. Before the operation, this recipient had a slight ST elevation, but graft function
was good immediately after the operation. He died of sudden cardiac arrest. This prompted us to adopt
stricter preoperative screening criteria. Patients with severe heart disease are now not recommended for
SPKT, and patients with mild heart disease should be selected carefully. All patients must reside in the
intensive care unit for at least 1 day post-surgery.
The pancreas, which is an organ of low blood flow, is prone to thrombosis after transplantation and
so thrombosis is one of the major reasons for loss of function. In our center, the vascular complication
rate was 14.3%. Gruessner et al reported a 12% rate of vascular thrombosis in a series of 445 consecutive
pancreatic transplantations,7 and Michalak et al described 12 pancreatic graft losses in 51 SPKT (23%)
after 1 year due to vascular thromboses.8 Our experience has taught us to trim the pancreas better, to keep
a suitable portal vein length of about 2.5 cm (or a length that is easy to bend around the head of the
pancreas), to make the blood vessel anastomoses with a well-distributed needle distance and edge
distance, to use venous heparin (100 U/hr) routinely for 4–7 days after the operation and to monitor the
blood flow within the transplanted organ twice a week.
In a report by Heredia et al., duodenal segment leaks occurred in 5%–20% recipients with
bladder-drainage and in 5%–8% recipients with enteric-drainage.9 There are a number of reasons for this,
including acute rejection, duodenal enteritis caused by cytomegalovirus, and chronic duodenal ulcer.10 In
patients with bladder drainage, the most common technical complication is a leak at the duodenal
segment.5 Surgical repair is rarely successful, as we experienced with one of our patients. However,
conservative treatment with Foley drainage can result in the closure of some leaks. On occasion, the
diagnosis of a leak is difficult and several detection methods have been described. Eckhoff et al reported a
high detection yield using nuclear imaging techniques.11 However, in our center, we examine the amylase
levels in the wound drainage fluid and use cystography to identify the specific location of the duodenal
segment leak. Four of our recipients suffered duodenal stump leaks, and all died after surgery. One had a
fistula of the duodenal stump about 18 days after the operation. He manifested with high fever, abdominal
pain and rebound tenderness, and cystography suggested a fistula of the duodenal stump. A catheter was
placed to drain the fluid, but did not work well. So, we decided to repair the leak. However, during the
operation, the ascending colon was damaged due to severe adhesions, and the patient experienced an
intestinal leak after the operation and died. Up until his death the graft function was good, blood glucose
levels were stable and kidney function was good. Two recipients died from erosive hemorrhage, while
another died from septic shock. Leakage of the duodenal stump is a severe complication after SPKT.12
Prevention is very important and a satisfactory blood supply to the duodenum should be ensured. Good
anastomotic technique is also critically important.
During the first months, SPKT recipients with bladder drainage may experience metabolic acidosis
and dehydration. The main cause of this is the loss of bicarbonate and fluid from the pancreas via the
urine. Grussner et al reported a 12% conversion rate from bladder drainage to enteric drainage because of
metabolic complications within 2 years after SPKT.13 During the early period after SPKT we give a daily
intravenous infusion of 5% NaHCO3 (250 ml) to prevent acidosis and dehydration. When the recipient is
discharged from hospital, oral NaHCO3 (12–20 g/day) is recommended. Three of our recipients had
several episodes of acidosis and dehydration, which manifested as inertia and a blood CO2CP 15–19
mmol/l. All recovered after bicarbonate and fluid therapy.
The morbidity associated with reflux pancreatitis after SPKT with bladder drainage is 11%–17%14
and it can occur at any time after the withdrawal of the urinary catheter, even up to several years later.
Pancreatitis is induced by the reflux of urine through an incompetent sphincter of Oddi.15 The graft
function is good with stable blood glucose levels and hemodialysis is unnecessary for the first 5–7 days
after the operation. Serum amylase returns to normal within 3 days. Reflux pancreatitis was found in three
recipients 2 weeks to 2 months after the operation. These recipients had a sudden high fever (up to 39°C),
with abdominal pain, tenderness, serum amylase of 160 U/l, and no fluid around the pancreas. These
recipients recovered with bladder catheterization and suitable antibiotics.
Intestinal drainage along with technological advances in surgery, will result in reduced surgery time,
less trauma and less risk of intra-abdominal infection, and will be widely used in major surgical
procedures. To improve the success rate and ensure a more straightforward operation, centers beginning
to carry out this operation should adopt the bladder drainage approach.16
A number of centers choose an immunosuppressive regimen of tacrolimus and mycophenolate
mofetil. As a result, the survival rates for kidney and pancreas grafts can be 100% and 80%, respectively,
at 1 year.17 Some reports suggest that this protocol can reduce the incidence of acute rejection,18 thus
making steroid-free maintenance a feasible option.19 Immunosuppression allows the efficient control of
rejection in SPKT patients. However, in our center, the incidence of acute rejection was high (42.9%).
Three kidneys and two pancreases were lost through acute and/or chronic rejection. These results are not
consistent with the decreased immunological failure rate (2%) for SPKT reported to the IPTR between
2000 and 2004.3 However, many factors such as poor economics or a low ratio of HLA matches may
affect the recipients’ prognosis.
We performed transplantations in 14 patients with type-2 diabetes mellitus. Eleven patients did well,
with normal glycemic parameters at follow-ups 1–9 years later. These results mirror those of Nath et al.,20
who transplanted 17 pancreases into patients with type-2 diabetes, including seven SPKT, four pancreas
after kidney, and six pancreas-alone transplants. Regarding the seven SPKT patients, they describe a 94%
survival rate for both patients and grafts at 1 year, which decreased to 74% at 4.3 years. Another study2
analyzed 135 SPKT transplants, 1/3 of which were performed in type-2 diabetic patients. They observed
5-year patient, pancreas, and kidney survival rates of 73%, 67%, and 72%, respectively. These results
confirm that long-term results in type-2 are comparable to those observed in transplant recipients with
type-1 diabetes.
SPKT patients are complex, presenting with difficult complications. In China, few centers carry out
this work. However, SPKT is a valid therapeutic option for uremic diabetics. Comprehensive
perioperative management, prevention and specific and timely treatment of complications, and effective
application of immunosuppressants are important factors affecting the outcome and long-term survival of
both grafts and patients. We also conduct a rigorous follow-up, consult with the transplant doctors by
telephone, and perform blood tests at least once a month and a cystoscopy every 6 months. Experience
will increase as more SPKT procedures are performed.
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