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Perit Dial Int 29(5): 517-522
2009
© 2009 International Society for Peritoneal Dialysis
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Clinical Sciences

COMPUTED TOMOGRAPHIC FINDINGS CHARACTERISTIC FOR ENCAPSULATING PERITONEAL SCLEROSIS: A CASE-CONTROL STUDY

Anniek Vlijm1, Jaap Stoker2, Shandra Bipat2, Anje M. Spijkerboer2, Saffire S.K.S. Phoa2, Robbert Maes3, Dirk G. Struijk1,4 and Raymond T. Krediet1

Division of Nephrology,1 Department of Medicine, and Department of Radiology,2 Academic Medical Center, University of Amsterdam, Amsterdam; Department of Radiology,3 Gemini Hospital, Den Helder; Dianet Foundation,4 Utrecht–Amsterdam, The Netherlands

Correspondence to: A. Vlijm, Department of Nephrology, Academic Medical Center, Meibergdreef 9, Room A01-111, 1105 AZ Amsterdam, The Netherlands. a.vlijm{at}amc.uva.nl


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 DISCLOSURE
 REFERENCES
 

{diamondsuit} Background: Computed tomography (CT) is often used to confirm the diagnosis of encapsulating peritoneal sclerosis (EPS) but there is no consensus on specific CT abnormalities. To establish CT findings characteristic for EPS, we compared CT findings between EPS patients and long-term peritoneal dialysis (PD) patients without EPS.

{diamondsuit} Methods: We included as cases all EPS patients in our center from 1996 to 2008 that underwent a CT scan at the time of diagnosis. Controls were all other long-term PD patients (PD duration ≥ 4 years) without EPS that had a CT scan for different reasons. The CT scans were blindly and independently reviewed by 3 radiologists: 2 abdominal radiologists with PD knowledge (Observers 1 and 2) and 1 radiologist without PD experience (Observer 3).

{diamondsuit} Results: We included 15 EPS patients and 16 controls. Observer 1 found 6 CT findings that were significantly more often present in EPS than in controls (p ≤ 0.05): peritoneal enhancement, thickening, and calcifications; adhesions of bowel loops; signs of obstruction; and fluid loculation/septation. Observer 2 scored almost identically but Observer 3 scored differently. The sensitivity and specificity of a combination of specific CT findings were, respectively, 100% and 94% for Observers 1 and 2, and 79% and 88% for Observer 3.

{diamondsuit} Conclusion: CT scans showed characteristic abnormalities that were significantly more often present in EPS patients compared to long-term PD control patients. CT can be used to confirm the diagnosis of EPS when experienced radiologists apply a combination of specific CT findings.

KEY WORDS: Encapsulating peritoneal sclerosis (EPS); computed tomography (CT); case-control study.

Long-term peritoneal dialysis (PD) can lead to functional and morphological changes in the peritoneum (1–4). The most severe complication is encapsulating peritoneal sclerosis (EPS), a rare condition in which the bowel loops are entrapped in a dense cocoon of fibrous tissue (5). The exact mechanism leading to the development of EPS has not yet been identified (6). Risk for EPS increases with duration of PD (7,8) and it frequently occurs after discontinuation of PD (7,9,10). The consequences for patients are enormous: progressive malnutrition due to repeated bowel obstruction, sepsis, and eventually even death in a substantial number of cases (7–12). In addition to duration of PD, exposure to dialysis solutions with high glucose/glucose degradation product concentration is considered a risk factor for the development of EPS (13). Kidney transplantation was recently suggested as another possible risk factor for developing EPS (14). The diagnosis of EPS is based on clinical symptoms in combination with pathological findings and abdominal imaging (15), but these techniques do not allow unambiguous diagnosis.

Although abdominal imaging is used to confirm the diagnosis of EPS, there is no consensus on specific radiological abnormalities. Ultrasonography shows signs of adhesions, small bowel dilatation, and typical thickening of the intestinal wall (16), but interpretation of the images is very dependent on the radiologist and there are no data on reproducibility. Use of computed tomography (CT) to diagnose EPS was introduced in 1988 (17) and the technique has been markedly improved since then (18). Although some case reports describe CT findings in EPS patients (19–23), there are only a few studies that describe larger patient groups (24) and only two studies in which CT scans of EPS patients are compared to those of other PD patients (25,26). In a case-control study by Stafford–Johnson et al., CT findings of 10 EPS patients were compared to those of 71 control patients on PD from 1 month to 7 years (25). These authors concluded that peritoneal calcifications, peritoneal thickening, fluid loculation, and tethering of small bowel loops should be considered diagnostic for EPS. Tarzi et al. recently studied abdominopelvic CT scans of 27 patients with EPS and compared them with CT scans of 15 hemodialysis and 20 PD patients using a scoring system. A strongly significant difference between total CT scan scores at diagnosis of EPS and total CT scan scores of controls was found (26).

Encapsulating peritoneal sclerosis occurs mainly in long-term PD patients. Little is known about the occurrence of CT abnormalities in long-term PD patients without EPS; therefore, a control group should consist of long-term PD patients exclusively, since we cannot exclude that chronic PD per se might cause abnormal CT findings. The aim of the present study was to compare CT findings in EPS patients with CT findings in long-term PD patients without EPS. Our research question was, Are there CT abnormalities that are characteristic for EPS? To answer this question, we designed a retrospective case-control study and included all EPS patients as cases and all other long-term PD patients with an available CT scan as controls.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 DISCLOSURE
 REFERENCES
 
PATIENTS
We included as cases all EPS patients with an available CT scan from around the time of diagnosis but before surgical confirmation. The patients had been treated from 1996 until October 2007 in our center, an academic medical center with a large PD population (of, on average, 60 prevalent PD patients). EPS was defined as a macroscopically confirmed condition of encapsulating sclerosis, or a clinically evident presentation with symptoms such as repeated bowel obstruction, nonresolving peritonitis, and ultrafiltration failure. For controls, we included all long-term PD patients (on PD for at least 4 years) from the same period without clinical signs of EPS and with an available CT scan done for different reasons.

REVIEW OF THE CT SCANS
Cases and controls were put in random order and 3 experienced radiologists were asked to independently and blindly review the CT scans. The radiologists were not aware of the prevalence of EPS in this study. Two of the radiologists were abdominal radiologists from our center with, respectively, 15 and 13 years of clinical experience (Observers 1 and 2). Each had seen a small number of the CT scans previously but the interval to the current reading was at least 2 years. Therefore, the chances of recall bias were considered negligible. The third observer was a radiologist with 10 years of clinical experience but from a small general hospital without PD patients (Observer 3).

Based on literature and in cooperation with these radiologists, we developed a score form on which eight items could be scored as present, absent, or unable to evaluate. The items were peritoneal enhancement, peritoneal thickening, peritoneal calcifications, large bowel wall thickening, small bowel wall thickening, adhesions of bowel loops (e.g., indrawing to the center of the abdominal cavity), signs of bowel obstruction (e.g., bowel dilatation), and fluid loculation, including septation.

STATISTICS
Clinical characteristics of both patient groups are presented as means and standard deviations. Ages are presented as means with ranges. Differences in clinical characteristics between the cases and controls were analyzed with independent sample t-tests. Differences in CT findings were analyzed with chi-square statistics or Fisher's exact probability tests. To analyze interobserver variability we determined means of agreement between the 3 radiologists. We combined specific CT findings and calculated sensitivity and specificity.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 DISCLOSURE
 REFERENCES
 
PATIENTS
We were able to include 15 EPS patients: 8 men and 7 women, mean age 43 (range 18 – 73) years, mean duration of PD 98 ± 34 months. The indications for the CT scans were suspicion of EPS in 7, abscesses or hematomas in 5, tumor in 1, bowel perforation in 1, and in 1 case the indication was not specified. In 10 of these patients the diagnosis was macroscopically confirmed during abdominal surgery. In 1 patient the diagnosis was macroscopically confirmed during autopsy. Mean time between the CT scan and macroscopic confirmation of EPS was 70 ± 67 days. In the remaining 4 patients there was strong clinical evidence for EPS: signs of repeated bowel obstruction, nonresolving peritonitis, ultrafiltration failure, severe weight loss, and bloodstained effluent. These symptoms could not be explained by another underlying condition. Eight patients developed EPS after discontinuation of PD: 5 patients had already transferred to hemodialysis and 3 patients had been transplanted. During follow-up until June 2008, 7 patients died because of EPS, which corresponds to a mortality of 47%. The remaining 8 patients were either on hemodialysis (n = 4) or had a functional kidney transplant (n = 4).

We were able to include 16 patients as controls: 7 men and 9 women, mean age 54 (range 32 – 78) years. Mean duration of PD was 62 ± 14 months, which was significantly lower compared to the EPS group (p ≤ 0.001). The underlying reasons for the CT scan were peritonitis in 5, suspicion of abscesses or hematomas in 4, and leakage of peritoneal fluid, diverticulitis, ultrafiltration failure, abdominal aortic aneurysm, gastric malignancy, bowel ischemia, and liver ischemia in 1 each. None of the control patients developed EPS during follow-up to June 2008. Nine patients died due to other causes, 6 patients were successfully transplanted, and 1 patient was transferred to hemodialysis.

REVIEW OF THE CT SCANS
A total of 31 CT scans (15 EPS patients and 16 controls) were reviewed. Almost all scans were spiral CT scans with a slice thickness of 5 – 5.5 mm. Two thirds of all patients had received intravenous contrast medium. The results of the 3 observers are summarized in Table 1. The scores are expressed as the number of positive findings for each specific item, followed by the number of scans that could be evaluated according to the radiologist. Figures 1(a) and 1(b) show the percentage of positive findings for each specific item per patient group and per observer.


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  		TABLE 1 Computed Tomographic Findings of Encapsulating Peritoneal Sclerosis (EPS) Patients and Controls by the Three Observers

 

Figure 1
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  		Figure 1 — Computed tomographic findings are represented as percentage of positive findings in EPS patients (black bars) and in controls (white bars). The number above each bar represents the observer (1, 2, or 3). Significant differences between patient groups are marked with asterisks: *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001. EPS = encapsulating peritoneal sclerosis.

 

In the readings by Observer 1, six CT findings were significantly more often present in EPS patients compared to controls: peritoneal enhancement, thickening, and calcifications; adhesions of bowel loops; signs of obstruction; and fluid loculation and/or septation. Observer 2 confirmed most of these findings but did not find a significant difference in peritoneal calcifications between the patient groups. Observer 3 had three CT findings that were significantly more often present in EPS: peritoneal thickening, calcifications, and adhesions. Agreement of scoring when all the separate items were taken into account was 90% between Observers 1 and 2, 75% between Observers 1 and 3, and 75% between Observers 2 and 3. Table 2 shows the percentage of agreement between the 3 observers per item. Differences in scoring among the observers were found mainly for peritoneal thickening and small bowel wall thickening. Localization of the thickened peritoneum was sometimes parietal, sometimes visceral, and, in some cases, both.


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  		TABLE 2 Percentage Agreement Between the Three Observers

 

No single item could distinguish definitely between EPS and controls with the exception of fluid loculation and/or septation according to Observers 1 and 2 [Figures 2(a) and 2(b)]. However, this was present in only one third of the EPS patients. None of the observers found significant differences in large and small bowel wall thickening between the groups; therefore, we combined the remaining six items (peritoneal enhancement, thickening, and calcifications; adhesions of bowel loops; signs of obstruction; and fluid loculation/septation) to calculate sensitivity and specificity of the CT scan for diagnosing EPS. For this calculation, a gold standard was required. Since the diagnosis of EPS was not doubtful in any of the cases and was macroscopically confirmed in 73%, this "certain diagnosis" was used as the gold standard. When the cutoff point for a positive CT scan was arbitrarily set at positively scoring for at least three of six items (and two of five items when no contrast enhancement was used), the sensitivity and specificity were 100% (15/15) and 94% (15/16) for Observers 1 and 2, and 79% (11/14) and 88% (14/16) for Observer 3.


Figure 2
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  		Figure 2 — An example of a computed tomography (CT) scan of a patient with encapsulating peritoneal sclerosis (EPS) and a kidney transplant shows signs of fluid loculation, septation, peritoneal enhancement, and indrawing of bowel loops to the center of the abdominal cavity (A). An example of a CT scan of an EPS patient shows evident septation in the ascites but no fluid loculation (B). The peritoneum is enhanced and bowel loops are drawn into the center of the abdominal cavity.

 


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
DISCLOSURE
 REFERENCES
 
Two abdominal radiologists from an academic medical center with a large PD population found that peritoneal enhancement and thickening, adhesions of bowel loops, signs of obstruction, and fluid loculation and/or septation are CT abnormalities characteristic for EPS. Observer 1 also found that peritoneal calcifications are characteristic for EPS. Observer 3, who is a general radiologist from a hospital without PD patients, scored differently from the 2 abdominal radiologists. This suggests that interpretation of CT scans from PD patients is difficult when experience with a PD population is lacking.

The CT findings that are considered characteristic for EPS were also found in some of the control patients. The "positive predictive value," the most important measure of a diagnostic method, could not be calculated because its value depends on the prevalence of the disease. Therefore, we developed a combination of CT findings and calculated sensitivity and specificity of the CT scan for diagnosing EPS. This combination was associated with very high sensitivity and specificity; however, it was developed in our EPS population and has not yet been tested in other populations.

According to the abdominal radiologists, peritoneal enhancement was very specific to EPS (p < 0.001); therefore, CT with contrast enhancement should be preferred. This enhancement, caused by perfusion of peritoneal vessels, might be due to an increased vascular peritoneal surface area (3). An inflammatory component as a cause of enhancement is not necessarily present in EPS (15).

The weakness of this study is that our control patients had a significantly shorter duration of PD than our EPS patients, although an inclusion criterion was having at least 4 years of PD. This is not surprising since long-term PD is a risk factor for developing EPS (7,8). However, none of the control patients developed EPS during follow-up. Another limitation of this study is that four cases of EPS were not macroscopically confirmed but these patients suffered from severe symptoms that could not be explained by another underlying disease. In 2000, an International Society for Peritoneal Dialysis ad hoc committee emphasized that the value of clinical symptoms of EPS should not be underestimated (15). Summers et al. described in their single-center experience of EPS that there is a spectrum of severity in this condition. The EPS patients were divided into a severe group, in which patients developed any standard surgical indication for laparotomy, and a mild/moderate group (12). In our study we did not find it necessary to divide our EPS patients into different groups because we found CT findings specific to EPS with very high sensitivity and specificity without this distinction.

It is important to have a proper tool to diagnose EPS because it can enable guidance of treatment. We also believe that delayed diagnosis limits the success of therapy and that patient outcome will improve when therapy is given at an early stage. There is some evidence that patients may benefit from immunosuppressive therapy (27,28) and from surgical treatment by surgeons with expertise in adhesiolysis in EPS (29). There is also some evidence that patients can be treated successfully with tamoxifen (12,30–32) and with supportive therapy such as total parental nutrition (8).

To our knowledge, no case-control studies have been published with a similar long-term control group (at least 4 years of PD); therefore, previous studies could not exclude the possibility of having CT abnormalities in long-term PD patients without EPS. In the present study, comparison between EPS patients and long-term PD patients without EPS was made: CT findings characteristic for EPS were found. We conclude that contrast-enhanced CT has high sensitivity and specificity for diagnosing EPS, especially when the scans are evaluated by experienced abdominal radiologists. Future studies should focus on validating the CT scan as a diagnostic tool in other populations of EPS patients. Also, the value of regular CT scanning in long-term PD patients can be studied using the combination of criteria developed in the present study.


   DISCLOSURE
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURE
REFERENCES
 
The authors declare no financial conflict of interest.

Received 17 July 2008; accepted 15 October 2008.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURE
 REFERENCES
 

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