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Oules R, Challah S, Brunner FP. Case-control study to de- termine the cause of sclerosing peritoneal disease. Nephrol Dial Transplant 1988; 3:66–9. 4. Nomoto ...

Peritoneal Dialysis International, Vol. 26, pp. 224–230 Printed in Canada. All rights reserved.

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FLUORODEOXYGLUCOSE POSITRON EMISSION TOMOGRAPHY DETECTS THE INFLAMMATORY PHASE OF SCLEROSING PERITONITIS

Ruth M. Tarzi,1 John W. Frank,2 Sohail Ahmad,1 Jeremy B. Levy,1 and Edwina A. Brown1 Renal Unit1 and Department of Nuclear Medicine,2 Charing Cross Hospital, London, United Kingdom

Perit Dial Int 2006; 26:224–230

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KEY WORDS: Sclerosing peritonitis; encapsulating sclerosing peritonitis; FDG-PET scan; complications of peritoneal dialysis. Correspondence to: R. Tarzi, Department of Renal Medicine, Hammersmith Hospital, Du Cane Road, London, W12 0NN, United Kingdom. [email protected] Received 30 March 2005; accepted 11 July 2005. 224

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eritoneal dialysis (PD) is an important form of renal replacement therapy. Sclerosing peritonitis (SP) is a rare but devastating complication in patients on PD, in which the peritoneum becomes progressively thickened and scarred, enclosing the bowel in fibrous tissue. Clinically, the patient presents with recurrent small bowel obstruction, bloody dialysis effluent or ascites, and malnutrition (1,2). The incidence in PD patients is generally around 1% – 3%, although some centers have reported higher rates (2–6). A recent prospective study of 1958 Japanese patients found that incidence rates rose steadily in patients on PD for longer than 5 years. Patients who developed SP after longer periods on PD also had a higher mortality rate. The overall mortality rate was high, at 37.5% (6), and these deaths were related mostly to bowel obstruction, malnutrition, and complications of surgery. Some investigators have described distinct phases of SP (7). First they describe an “inflammatory” phase, characterized by peritoneal inflammation, raised inflammatory markers, and low grade fever, followed by irreversible scarring and bowel adhesions, an “encapsulating” stage. It would be advantageous to identify patients at the earliest stage of the disease, before irreversible scarring occurs. However, the early clinical features of SP may be nonspecific and are often not recognized until the patient develops complications such as bowel obstruction and abdominal collections. The findings of peritoneal calcifications on plain abdominal radiography and thickened peritoneum seen on computed tomography (CT) have classically been used to support the diagnosis (8,9). However, these changes occur later in the disease, when therapeutic maneuvers, such as stopping PD, or pharmacological interventions may be less effective. Therefore, a means to identify patients at an earlier inflammatory stage of the disease is required. The introduction of functional imaging techniques such as 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) has enabled the identification of

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♦♦Objective: We studied the effectiveness of 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) in detecting inflammation in known or suspected cases of sclerosing peritonitis in patients on peritoneal dialysis (PD). ♦♦Design: We undertook FDG-PET scanning in PD patients presenting with symptoms or signs suggestive of sclerosing peritonitis (SP), and in patients on long-term PD with no symptoms of SP. ♦♦Setting: The study was performed in a PD unit in a tertiary-care hospital. ♦♦Patients and Methods: Three patients with known or strongly suspected SP underwent FDG-PET scans, 1 within 3 months of presentation with symptoms and 2 who were scanned more than 9 months after presentation. One patient was scanned at an early and a late time point. Five patients who had been on PD for more than 5 years and who were asymptomatic also underwent FDG-PET scanning. Scans were interpreted by a specialist in nuclear medicine. ♦♦Results: The scan performed in the early stages of SP showed increased peritoneal uptake. However, three scans taken more than 9 months after presentation with suspected SP showed mild peritoneal abnormalities only. One of 5 asymptomatic long-term PD patients showed increased peritoneal uptake associated with loss of ultrafiltration and high transporter status. ♦♦Conclusions: FDG-PET scanning may be a useful adjunct in the diagnosis of the acute phase of SP. More study is needed to define its role in the diagnosis of SP in asymptomatic PD patients.

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METHODS Patients with suspected SP were identified for FDGPET scanning from the clinical PD program at Charing Cross Hospital, London, UK. Criteria for inclusion included recurrent, resistant, or loculated sterile ascites (especially after cessation of PD as a mode of renal replacement therapy), recurrent abdominal pain, or small bowel obstruction. All of the patients with suspected SP had a background of long-term PD, high transport status, and low ultrafiltration. Five asymptomatic patients from our unit who had been on PD for more than 5 years were also scanned. One of these (Patient 4) had low ultrafiltration and high transport status and had been on PD for 10 years, but had no symptoms of SP. Informed consent was obtained. Patients were referred to the Department of Nuclear Medicine for an FDG-PET scan using a Siemens ART halfring scanner (Siemens, Bracknell, UK). Each scan took 1 1/2 hours with 7 bed positions. The injected dose of 18FDG varied between 164 MBq and 211 MBq, and the patients’ circulating glucose levels were between 3.2 and 5 mmol/L. The data were reconstructed using the Siemens software and attenuation correction provided by the machine’s 137Cs sources. The patients were all fasted

for 6 hours prior to injection and then rested in a darkened quiet room. Imaging was commenced 1 hour post injection. The patients did not have PD fluid in the abdomen at the time of imaging. The PET scans were reported by an experienced nuclear medicine consultant (JWF) and note was made of the standard uptake values (SUV), which varied between 1.7 and 3.3. In general, the SUV were those associated with inflammatory change. RESULTS PATIENT 1

Patient 1 presented in 1996 at the age of 19 with endstage renal failure (ESRF) of uncertain etiology. She started continuous ambulatory PD (CAPD) in 1996 and changed to automated PD (APD) in 1998 to improve clearance and fluid removal. Six years later, in October 2002, she presented with her first episode of peritonitis with coagulase-negative staphylococcus. This did not respond adequately to treatment with antibiotics and the PD catheter was removed on day 4. Despite this, she continued to have fever and abdominal pain and, 8 days after the removal of the catheter, she underwent a second laparotomy, which showed matted loops of bowel with adhesions. Peritoneal biopsies were not taken. One month later, she presented with a loculated abdominal fluid collection and then developed subacute bowel obstruction. Cultures of the abdominal fluid were negative for bacteria, fungi, and acid-fast bacilli. At this stage, the first FDG-PET scan was performed [see Figure 1(a)], showing well-defined uptake over the peritoneal surfaces in the abdomen. An abdominal CT scan taken at the same time showed peritoneal calcification and thickened bowel loops [Figure 1(c)]. Over the next few months, she had recurrent episodes of small bowel obstruction necessitating hospital admission. In April 2003, she was started on tamoxifen 20 mg daily for presumed inflammatory SP. Since that time, there has been a reduction in the frequency of her admissions with bowel obstruction. The second FDG-PET scan was taken 19 months after her initial presentation with loculated fluid collections and subacute bowel obstruction, and showed a considerable reduction in peritoneal uptake [Figure 1(b)]. The SUV were high (3.3) over the anterior peritoneum at presentation, falling to 1.7 after 19 months. PATIENT 2

Patient 2 is a 49-year-old Zimbabwean man with ESRF secondary to biopsy-proven HIV nephropathy. He had a history of sarcoidosis, diagnosed in 1993, and a 225

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areas with high metabolic activity within the body. FDGPET uses a radioactively labeled tracer (18F-fluorodeoxyglucose). This tracer is taken up by tissues that are avidly utilizing glucose, for example neoplastic or inflammatory lesions. FDG-PET is useful in detecting these inflammatory and neoplastic conditions before gross structural abnormalities become evident (10). FDG-PET has been used extensively in the oncology field in staging tumors (especially lymphomas), monitoring response to treatment, and detecting recurrence. The present study aims to detect whether FDG-PET can detect increased metabolic activity in the peritoneum during the inflammatory phase of SP. Labeled white cell scanning is an alternative means of identification of inflammatory foci. However, as the patients’ white counts were within the normal range, it was felt that performing a labeled white cell scan would have a very low likelihood of success, and we felt that PET imaging would give greater sensitivity. The first three cases illustrate the use of FDG-PET in combination with abdominal CT in the investigation of patients with suspected SP (Patients 1 to 3). Patients 4 to 8 are PD patients without symptoms of SP who have been on PD for more than 5 years and are therefore at risk of developing the disease. Patient 4 was specifically selected because he had been on PD for more than 10 years and had a high transport status.

PET SCANS IN SCLEROSING PERITONITIS

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A

B

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and then 6 weeks following this, he developed left flank pain and a large abdominal mass [Figure 2(a)]. This drained sterile blood-stained ascites and he has since had recurrent collections and episodes of subacute bowel obstruction. Cultures of the ascites were negative for bacteria, fungi, and mycobacteria, and scanty white cells only were seen. He was started on tamoxifen at this time. The FDG-PET scan was taken 9 months after the patient first presented with symptoms suggestive of SP [Figure 2(b)]. At this stage, there was mildly increased uptake in the abdomen, with evidence of large fluid collections. A

high-grade lymphoma in 1999, treated with radiotherapy and chemotherapy, neither of which was currently active. He started PD in January 2000 and his initial course was unremarkable. He had one episode of peritonitis secondary to a coagulase-negative staphylococcus in July 2002, which was successfully treated with antibiotics. However, in August 2003, he developed peritonitis secondary to methicillin-resistant Staphylococcus aureus (MRSA), which necessitated removal of the PD catheter and conversion to hemodialysis. Two weeks later, he presented with an episode of subacute bowel obstruction, 226

B

Figure 2 — Imaging for Patient 2: Contrast-enhanced computed tomography of the abdomen of Patient 2 shows loculated abdominal collection (arrow) (A). Maximum intensity projection FDG-PET scan shows evidence of loculated abdominal collections (arrows) but only mildly increased peritoneal uptake (B).

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Figure 1 — Imaging for Patient 1: Coronal, axial, and sagital FDG-PET scan taken 2 months after clinical presentation with sclerosing peritonitis (A). There was increased tracer uptake in the peritoneum (arrows). Corresponding coronal, axial, and sagital FDG-PET scans taken 19 months after clinical presentation with sclerosing peritonitis show reduced peritoneal uptake compared with the previous scan (B). Abdominal nonenhanced computed tomography taken around the time of original presentation with sclerosing peritonitis shows peritoneal calcification, dilated small bowel loops, and thickened peritoneum (C). FDG-PET = 18F-fluorodeoxyglucose positron emission tomography.

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PET SCANS IN SCLEROSING PERITONITIS

PATIENT 4

Patient 3 is a 57-year-old Somali man who presented with ESRF of uncertain etiology, small kidneys, and a history of hypertension. He started hemodialysis in 1997 but, due to multiple failed fistula attempts, converted to CAPD in 1998. He was fully treated for tuberculous lymphadenitis in August 1998. In September 2000 and April 2001, he had two episodes of PD peritonitis that were successfully treated with antibiotics. However, in October 2001, he presented with peritonitis due to Klebsiella pneumoniae, which did not respond to medical treatment; the PD catheter was removed 6 days after presentation and he was converted to hemodialysis. One month later, he presented with persistent ascites that did not resolve for over 6 months [see Figure 3(a)]. The ascites was sterile, with no bacteria or mycobacteria cultured. Gradually, his symptoms and ascites have started to resolve spontaneously [repeat CT 1 year later shown in Figure 3(b)]. The FDG-PET scan was undertaken in May 2004, 32 months after his initial presentation. At this stage, there was only mildly increased uptake in the abdomen [Figure 3(c)].

Patient 4 presented at the age of 37 with ESRF of uncertain etiology, hypertension, and small kidneys. He commenced PD in June 1993. He has remained on PD since that time and has had only 1 episode of bacterial peritonitis (in October 2000), with coagulase-negative staphylococcus, which was successfully treated with antibiotics. However, he had developed progressive loss of ultrafiltration (

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