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Vascular and Interventional Radiology |
1 From the Department of Radiology (T.D.A., B.G., J.W.C.), the Division of Nephrology and Internal Medicine (T.S.L., B.M.I.H.), and the Department of Surgery (M.D.S.), Mayo Clinic, 200 First St SW, Rochester, MN 55905. From the 2002 RSNA scientific assembly. Received February 19, 2003; revision requested May 7; revision received August 25; accepted October 8. Address correspondence to T.D.A. (e-mail: atwell.thomas@mayo.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Data from 232 percutaneous US-guided pancreas transplant biopsies performed in 88 patients were retrospectively reviewed. Biopsies were typically performed on an outpatient basis by using local anesthesia. Considerations included the indication for the biopsy, the type of pancreas transplant, the number of needle passes, the size of the biopsy needle, the use of aspirin, and the success of the biopsy. Important complications were detailed.
RESULTS: Of the 232 biopsies performed, 78 were for clinically indicated reasons and 154 were for surveillance purposes. The number of biopsy procedures per patient ranged from one to nine (mean, 2.6). Two needle passes were performed in 196 (84.5%) of the biopsy procedures. Almost all biopsies (ie, 228 [98.3%]) were performed by using an 18-gauge biopsy device. Adequate pancreatic tissue was obtained in 223 (96.1%) of the procedures. One hundred sixty-seven biopsies (72.0%) were performed while patients were receiving therapeutic aspirin. Six biopsies (2.6%) resulted in clinically important complications: three cases of intraabdominal hemorrhage and one case each of gross hematuria, allograft pancreatitis, and severe pain requiring overnight hospitalization. Two of the four bleeding complications occurred while patients were receiving therapeutic aspirin.
CONCLUSION: US-guided biopsy of pancreas transplants yielded tissue that was adequate more than 96% of the time. Important complications in this study were few (2.6%) and did not appear to be related to aspirin use.
© RSNA, 2004
Index terms: Biopsies, complications, 770.459, 770.715 • Drugs, side effects • Pancreas, biopsy, 770.1261 • Pancreas, transplantation, 770.1261, 770.455 • Ultrasound (US), guidance, 770.12985
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Although graft survival has improved, monitoring a pancreas allograft for rejection is difficult, particularly in patients who have undergone only pancreas transplantation and in patients who have undergone pancreas transplantation after kidney transplantation. In these patients, unlike in patients who have undergone simultaneous pancreas and kidney transplantation, renal function cannot be used as a measure of pancreas allograft status. Laboratory measures of pancreatic function, including serum and urinary levels of amylase and serum levels of glucose, are nonsensitive and nonspecific for rejection, and hyperglycemia usually develops only at a more advanced stage of rejection (2–4). In fact, acute rejection occurs in the absence of biochemical abnormalities in up to 40% of patients (5).
Ultrasonography (US) has been used in the evaluation of pancreas transplants. Gray-scale imaging is moderately specific but is not sensitive in depicting abnormalities suggestive of rejection (6). Considerable interest has been expressed in Doppler US imaging, although the role of the resistive index has been validated only in cases of severe acute or chronic rejection (7,8).
Because of the lack of both sensitivity and specificity associated with other measurements of rejection, the pancreas is often assessed histologically. There are several methods of obtaining pancreatic tissue. The two most common methods for obtaining needle biopsy specimens are the cystoscopic transduodenal approach and the percutaneous approach.
US is often used for percutaneous biopsy guidance because of its relatively low cost, lack of ionizing radiation, and real-time imaging capabilities. To date, there are few reports of large series in which this procedure was used, although in a recent review from the University of Maryland, an 88% success rate in obtaining adequate tissue for histologic analysis and a very low (2.8%) complication rate were reported (9). The purpose of our study was to retrospectively assess our experience with percutaneous US-guided biopsies of pancreas transplants.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Biopsy Procedure
For all patients, results from coagulation studies, including platelet count, prothrombin time, and activated partial thromboplastin time, were obtained before the biopsy was performed. One of several staff radiologists (n = 21, including T.D.A., B.G., and J.W.C.) with 1–24 years of experience in US-guided biopsy techniques obtained all of the biopsy specimens, except in a single case in which a senior trainee obtained the specimen with the close supervision of a staff radiologist.
Biopsy specimens were obtained by using an Acuson Sequoia US system (Siemens, Mountain View, Calif) with 8-MHz linear transducers or 6-MHz curved transducers. Typically, two samples were obtained from the transplant with the use of real-time US guidance, a freehand technique, and an automated biopsy device (Fig 1). Additional needle passes were made if there was doubt about the yield of the samples obtained. Rarely, a single needle pass was performed in those patients deemed to be at risk of bleeding. At our institution, we commonly use an 18-gauge Monopty biopsy device (C. R. Bard, Covington, Ga) that has a 22-mm penetration depth ("throw") and includes a 17-mm specimen trough.
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Patient medical records were reviewed by two of the authors (T.D.A. and B.M.I.H.). Considerations included the type of pancreas transplantation performed (ie, whether the pancreas was transplanted alone, after kidney transplantation, or at the same time as kidney transplantation and whether the pancreas transplant was bladder drained or enteric drained), the indication for biopsy, the number of biopsy procedures per patient, and the number of biopsy procedures per radiologist. We also reviewed the number of needle passes performed per biopsy procedure, the size of the biopsy needle used, the adequacy of the specimens (an adequate specimen was defined as one that contained enough pancreatic tissue to enable the pathologist to render a histologic diagnosis), and patient aspirin use.
Specific attention was directed toward important complications. Important complications were defined as biopsy-related events resulting in notable deviation from normal patient care and included events requiring overnight hospitalization, transfusion, or other notable interventions. For those patients hospitalized before the biopsy, notable deviation from scheduled care was considered an important complication. For those patients with important complications, the pertinent medical records and imaging data were thoroughly reviewed by five of the authors (T.D.A., B.G., T.S.L., J.W.C., and M.D.S.).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The number of biopsy procedures performed per patient ranged from one to nine (average, 2.6). The total number of biopsy procedures performed by each radiologist ranged from one to 43. The number of needle passes performed during the 232 biopsy procedures ranged from one to four, with 196 biopsies (84.5%) involving two needle passes. In 228 (98.3%) of the 232 biopsies, an 18-gauge automated biopsy device was used. The sizes of the devices used in the other four biopsies were 16 gauge for one biopsy, 19 gauge for one, and 20 gauge for two.
One hundred sixty-seven (72.0%) of the 232 biopsies were performed while patients were receiving therapeutic aspirin. Fifty-five of these biopsies (23.7% of the total number of biopsies) were performed when patients had taken aspirin on the day of the biopsy. The remaining 112 biopsies (48.3% of the total number of biopsies) were performed when patients had refrained from taking aspirin before the biopsy procedure.
Adequate pancreas allograft tissue was obtained in 223 (96.1%) of 232 biopsy procedures. The six biopsy procedures performed in enteric-drained transplants were successful. Seven staff radiologists with various levels of experience (1–20 years) independently performed the nine (3.9%) unsuccessful procedures. In eight of these procedures, an 18-gauge biopsy device was used, and in one procedure, a 20-gauge biopsy device was used. Five requested biopsies could not be performed because of poor visualization of the allograft or the intervening bowel (or both). These biopsies were not included in our analysis.
Six biopsies (2.6%) resulted in clinically important complications. Staff radiologists performed these six procedures, and the most experienced radiologist performed three of them. All six biopsies were performed on a protocol basis. The six complications occurred at various times after the biopsy specimens were obtained. Large hematomas developed in three patients, one of whom was a 43-year-old woman who had normal coagulation study results and was not receiving therapeutic aspirin. This woman underwent a protocol biopsy 7 days after receiving her allograft. Two needle passes into the graft were performed with an 18-gauge biopsy device. An hour after the biopsy specimen was obtained, she experienced severe abdominal pain, and a subsequent computed tomographic (CT) examination revealed a large intraabdominal perigraft hematoma (Fig 2). She required multiple blood transfusions during the subsequent 5 days.
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Other clinically important complications developed in three patients. One patient was a 43-year-old man in whom abdominal pain developed after the biopsy specimen was obtained. He had markedly elevated levels of serum amylase (2,574 U/L) and lipase (12,974 U/L) compared with preprocedure levels (75 U/L and 235 U/L, respectively). Postbiopsy allograft pancreatitis was diagnosed, and he was hospitalized for 3 days. The pancreatitis resolved uneventfully with conservative management.
The second patient was a 34-year-old woman with normal coagulation test results. Gross hematuria developed after two 18-gauge core specimens were obtained from the head of her pancreas transplant. She had refrained from taking therapeutic aspirin beginning 7 days before the biopsy. Because of the magnitude of the hematuria, she was admitted to the hospital for overnight observation. She remained hemodynamically stable, with stable serum levels of hemoglobin. Transfusion was not required, and she was dismissed from the hospital the next day.
The third patient was a 43-year-old woman in whom severe abdominal pain developed after the biopsy specimen was obtained. A CT examination revealed no hematoma. Her levels of serum amylase and lipase were unchanged from the levels before the biopsy. She was admitted to the hospital and observed overnight; her pain resolved spontaneously.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Because vascular changes occur within the graft during rejection, Doppler US analysis has been investigated as a tool for assessing graft status. In a study of 78 US-guided cystoscopic pancreas allograft biopsies, Nelson et al (8) were unable to show correlation of the resistive index with evidence of acute mild or moderate rejection, which was present at 38 of the biopsies (positive predictive value, 47%; negative predictive value, 43%). However, the mean resistive index was significantly higher in patients with chronic rejection (0.72) than in patients without rejection (0.65), patients with acute mild rejection (0.64), and patients with acute moderate rejection (0.63). There were no cases of severe rejection in their study.
Similarly, Wong et al (6) were unable to observe an appreciable role for the resistive index in the diagnosis of acute rejection in their series of 51 biopsies. Nevertheless, the resistive index may assist in the diagnosis of acute severe rejection: A mean resistive index of 0.85 was observed in two patients with pathologically proved disease in a series of 20 biopsies of pancreas transplants studied by Aideyan et al (7).
Histologic analysis is generally accepted to be the primary method of evaluating the pancreas allograft for evidence of rejection (10). Initially, open surgical biopsy was necessary for obtaining tissue. However, cystoscopic transduodenal and percutaneous biopsies have now become the standard of care.
Cystoscopic transduodenal biopsy yields adequate tissue for histologic analysis in 87% of procedures (11). This approach requires the use of an operating room and general anesthesia, resulting in considerable cost and expenditure of time. Patients are typically hospitalized overnight, regardless of the biopsy result. Despite the invasiveness of the procedure, important complications are rare (12). In their review of 103 cystoscopic transduodenal biopsies, Laftavi et al (11) reported that macroscopic hematuria occurred in 4% of cases, none of which required transfusion.
Percutaneous imaging-guided biopsy, performed either with CT or with US, is an effective means of performing a biopsy of the pancreas allograft. Laftavi et al (11) also reviewed their experience with CT-guided percutaneous biopsy of pancreas transplants. They performed 70 biopsies and successfully obtained pancreatic tissue for histologic analysis in 92% of the cases. However, 25% of the time they were unable to safely access the graft, and the biopsy could not be performed. Noteworthy hemorrhage occurred in two patients (3%).
Percutaneous US-guided allograft biopsy is recognized as a highly effective and relatively safe method of obtaining tissue for the histologic determination of rejection. The method was described by Allen et al (2) in 1991, and investigators have continued to have good success rates in obtaining allograft tissue. Lee et al (10) achieved an overall success rate of 83% in 42 US-guided biopsies, including 15 procedures involving prebiopsy localization of the transplant with CT. With US-guided biopsy alone, adequate tissue was obtained in 89% of the procedures. When CT localization was used in conjunction with US guidance, adequate tissue was obtained in only 73% of the cases. In their study, both 18- and 20-gauge biopsy needles were used, and a slightly higher success rate per core specimen (83% vs 76%) was observed with use of the smaller caliber device.
Recently, Klassen et al (9) reviewed data from 426 US-guided biopsies performed by nephrologists at their institution. With a strict definition of tissue adequacy, they achieved a success rate of 88% by using an 18-gauge biopsy device, typically obtaining only one core of tissue during the procedure. Using an average of two needle passes per biopsy procedure and an 18-gauge biopsy device, we were able to achieve a 96% success rate.
Our low rate of important complications (2.6%) is similar to the rate (1.9%) reported in the review by Klassen et al (9). In three biopsies, their investigators inadvertently sampled other organs, including the kidney, small bowel, and liver. Among our unsuccessful biopsies, one of the pathology specimens contained lymphoid tissue; the remainder of our nondiagnostic specimens consisted of fat or skeletal muscle.
There was no apparent association between aspirin use and the risk of bleeding in our study. None of the patients who received aspirin the day of the procedure experienced an important bleeding complication. Of the remaining patients who were receiving therapeutic aspirin, two experienced important bleeding complications. One patient had discontinued aspirin therapy the day before the procedure, and a second patient had stopped aspirin therapy a week before the biopsy was performed. The two other patients with bleeding complications were not receiving aspirin.
At this time, if clinically feasible, we prefer to withhold aspirin therapy for 1 week before the biopsy. In patients with a history or possibility of vascular compromise, the beneficial effect of aspirin overrides this concern for bleeding risk. In exceptional cases, a bleeding time may be obtained, although this test is of questionable value in determining bleeding risk (13,14).
Postbiopsy allograft clinical pancreatitis occurred in only one patient, and this resolved with conservative management. Pancreatitis has occurred after biopsy of normal native pancreas (15,16). Violation of normal pancreatic parenchyma most likely results in the release of enzymes along the needle track into the adjacent soft tissues, resulting in pancreatitis. Subclinical pancreatitis probably occurs frequently after biopsy, as demonstrated by the frequent finding of elevated levels of serum pancreatic enzymes after biopsy (2).
There were limitations to our study. We reviewed data only for biopsies that were performed; we did not include data for five biopsies that were canceled because of poor visualization of the allograft.
Twenty-one radiologists with a vast spectrum of technical experience performed the biopsies. Experience level did not appear to play a role in the success of our biopsies, because unsuccessful biopsies occurred across nearly all levels of experience.
We defined a successful biopsy as that which yielded enough pancreas transplant tissue for histologic diagnosis. We did not characterize the histologic sample further. Other investigators have been more precise in their definition, adopting criteria established by the University of Maryland (9). We have not been asked to repeat a biopsy when pancreas tissue is obtained.
We defined an important complication as a biopsy-related event resulting in notable deviation from our established protocol. We did not recognize isolated small perigraft collections of fluid as an important complication. These are frequently seen in asymptomatic patients and resolve with no consequence. We do not routinely measure levels of serum amylase or lipase after biopsy because they are frequently elevated in asymptomatic patients after a biopsy. Asymptomatic, spontaneously resolving hematuria also occurs in a few patients; it too was not considered an important complication in this study.
Because of the nonsensitivity of biochemical markers (eg, serum amylase, lipase, and glucose and urinary amylase), we have found surveillance biopsies to be important in identifying early, subclinical rejection in patients who have undergone pancreas transplantation only or pancreas transplantation after kidney transplantation (5). Given the low complication rate of US-guided pancreas allograft biopsies in our experience to date, we believe that surveillance biopsies are a relatively safe means of monitoring acute rejection in these patients.
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FOOTNOTES |
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