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Encapsulating peritoneal sclerosis: early diagnosis and risk factors

Sampimon, D.E.

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Citation for published version (APA):Sampimon, D. E. (2010). Encapsulating peritoneal sclerosis: early diagnosis and risk factors.

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87

CHAPTER 8

THE TIME COURSE OF PERITONEAL TRANSPORT PARAMETERS IN PERITONEAL DIALYSIS PATIENTS WHO DEVELOP

ENCAPSULATING PERITONEAL SCLEROSIS

Nephrology Dialysis Transplantation – in press

1 Department of Internal Medicine, Division of Nephrology, Academic Medical Center, University of Amsterdam

2 Dianet Foundation, Amsterdam-Utrecht, The Netherlands

Denise E. Sampimon1, Annemieke M. Coester1, Dirk G. Struijk1,2, Raymond T. Krediet1.

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ABSTRACT

ABstRAct

Background: Encapsulating peritoneal sclerosis (EPS) is a severe complication of peritoneal dialysis (PD). The first aim was to analyze the risk of EPS in patients who had developed ultrafiltration failure (UFF). The second aim was to identify specific peritoneal transport alterations that distinguish patients with UFF from patients who will develop EPS.

Methods: All patients of this study were treated with PD between July 1995 and December 2008 in the Academic Medical Center, Amsterdam, the Netherlands. Risk analysis: all PD patients who developed UFF after at least 2 years of PD. Peritoneal transport analysis: all patients who had PD for at least 55 months were included: 12 EPS patients, 21 patients with UFF and 26 patients with normal ultrafiltration (UF). The peritoneal function was measured yearly with a standard peritoneal permeability analysis. UFF was defined as net UF<400mL after a 4-h dwell with a 3.86% dialysis solution.

Results: Risk analysis: Of the 48 UFF patients 10 eventually developed EPS. Fifty percent of the patients who continued PD for more than three years after the establishment of UFF developed EPS. Peritoneal function analysis: No differences were present for the time courses of solute transport and fluid transport between the EPS and the UFF groups. Overall, the EPS and normal UF group had lower values for the effective lymphatic absorption rate (ELAR) than the UFF group.

Conclusions: The risk of EPS increases with continuation of PD while UFF is present. Transport characteristics are similar between EPS patients and UFF patients without this complication. A constantly low ELAR may distinguish the EPS patients from those with UFF only.

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intRODUctiOn

Encapsulating peritoneal sclerosis (EPS) is a rare but severe complication of long-term peritoneal dialysis (PD). Research focussing on early detection is of great importance for developing strategies to prevent EPS. The diagnosis of EPS is based on clinical signs and symptoms, mostly confirmed by radiological or macroscopic findings. The clinical symptoms include bowel obstruction, ascites and blood-stained effluent 1,2. Typical findings at laparotomy or autopsy are thickening of the bowel wall, mesentery and/or the parietal peritoneum, adherent bowel loops covered by thick fibrous tissue and bowel loops adherent to the abdominal wall with or without calcifications1,3,4. Ultrafiltration failure (UFF) is almost always present in patients who develop EPS 1,2,5,6. However, not all patients with UFF develop EPS. The risk of the development of EPS after UFF is diagnosed is unknown.

It is difficult to predict from functional parameters which patient will develop EPS, because hardly any longitudinal studies focussed on peritoneal transport preceding EPS, have been published. However, transport changes might be specific for the development of EPS.

The first aim of this study was to analyze the risk of EPS in patients who developed UFF after at least 2 years of PD. The second aim was to identify peritoneal transport alterations that may be specific for the development of EPS. We analyzed whether the longitudinal analysis of solute and fluid transport preceding the diagnosis of EPS could distinguish these patients from long-term patients with UFF and long-term patients with normal ultrafiltration (UF).

MetHODs

To answer both research questions, two separate analyses have been performed in patient groups selected on different criteria, as shown in Figure 1. The first analysis on the risk of EPS after the development of UFF (analysis A) followed patients from the start of UFF after at least 2 years of PD until the end of PD therapy. The second analysis about the peritoneal function alterations in EPS patients and controls (analysis B) applied a backward approach and included all patients who had completed at least 55 months of PD. This study was conducted according to medical ethical standards. In the Netherlands, retrospective data collection and, analysis of data obtained during normal patient care do not require approval from the committee of medical ethics. All data was kept under code.

Analysis A: risk of EPS after development of UFFTo analyze the risk of EPS in patients with UFF, we included all patients who developed UFF after at least two years of PD between July 1995 and December 2008. EPS patients were diagnosed in our department and selected for this study according to the procedure of Hendriks et al.1 In short, the diagnosis of EPS was based on clinical features (bowel obstruction, ascites and blood stained effluent almost always in combination with UFF) confirmed either by findings at radiology, laparotomy or autopsy and reviewed by two experienced nephrologists. Only patients who developed UFF after 2 years of PD were included because UFF within the first 2 years of PD is associated with co-morbidity and a high lymphatic absorption rate, while UFF in long-term PD is most often due to a decreased osmotic conductance to glucose7. UFF was defined

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according to the recommendation of the International Society for Peritoneal Dialysis, as net UF of < 400 mL/4h with a 3.86% glucose dwell8. Co-morbidity was expressed as the Davies score9. The risk of EPS after the development of UFF was expressed as a proportion of the total UFF population.

Analysis B: longitudinal analysis of peritoneal transportTo analyse the time course of peritoneal membrane parameters preceding the diagnosis of EPS, we included all adult EPS patients who were treated with PD between July 1995 and December 2008. Controls were divided into a normal UF group and a UFF group based on their last available standard peritoneal permeability analysis (SPA). A restriction of 55 months of PD treatment was applied because this was the shortest PD duration in the EPS group. The division in the control group was based on the net UF (400mL/4h/3.86%) of their last available SPA. Controls were included if they had at least one SPA with a 3.86% glucose dwell available. The number of SPAs per patient ranged from one to four. The mean interval between the SPAs was on average one year: the median interval to the diagnosis of EPS at Measure Point -1 was nine months, at Measure Point -2 was 22 months, at Measure Point -3 was 33 months and at Measure Point -4 was 47 months. This allowed us to express the measure points as years prior the diagnosis of EPS, whereas Measure Point 0 was the time of the diagnosis of EPS. None of the control patients developed EPS in the following 3 years after their study period.

ProcedureThe SPAs are performed yearly in all patients on a voluntary basis. The test is based on a 4-h dwell period10. Briefly, after a rinsing procedure, a fresh 3.86% glucose based dialysis solution (Dianeal®, Baxter HealthcareLtd., IRL) is instilled for a test dwell. Dialysate samples are taken before instillation and at multiple time points during the test (10, 20, 30, 60, 120, 180 and 240 minutes). After drainage at 240 min, the peritoneal cavity is rinsed with Dianeal similar to the start of the procedure. Samples from this bag are used to calculate the residual volume. Blood samples are taken at the beginning and at the end of the test. To calculate peritoneal fluid kinetics including the residual renal function, dextran 70, 1g/L(Hyskon, Medisan Pharmaceuticals AB, Uppsala, Sweden) is added to the test solution. To prevent a possible anaphylactic reaction to dextran 70, dextran 1 (Promiten, NPBI, Emmercompascuum, the Netherlands) is injected intravenously before instillation of the test solution11.

calculationsSolute and fluid transport parameters were calculated as described previously10,12. Transport of small solutes was calculated as mass transfer area coefficients (MTAC). The MTAC were calculated according to the model of Waniewski et al. and corrected for body surface area13. The solute concentrations in plasma were corrected for plasma water.

Peritoneal clearances were calculated for the following proteins: beta-2-microglobulin, albumin (alb), immunoglobulin G (IgG) and alpha-2-macroglobulin (A2m). They were corrected for body surface area. With the clearances of these four proteins the restriction coefficient, a functional characterization of the intrinsic peritoneal permeability, was calculated. The restriction coefficient is the slope of

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the power relation between the clearances of the above-mentioned proteins with different molecular weights and their free diffusion coefficients in water14,15.

The changes in intraperitoneal volume (IPV) result from transcapillary ultrafiltration (TCUF) and fluid absorption which includes lymphatic absorption, disappearance to the interstitial tissues and backfiltration into the capillaries. Changes in IPV during the dwell and TCUF were assessed with the intraperitoneal administered volume marker dextran 7016. The effective lymphatic absorption rate (ELAR) was calculated by taking the difference between the instilled and recovered dextran mass and divided by the geometric mean of the dialysate dextran concentration14. Net UF was calculated as the difference between TCUF at 240 min and lymphatic absorption at 240 minutes.

Free water transport (FWT) was calculated as described previously by Smit et al.17 by subtracting solute-coupled water transport, which is fluid transport through the small pores, from TCUF. A correction for sodium diffusion was performed using the MTAC of urate18.

statistical analysisData are presented as medians and ranges, unless stated otherwise. A cross-tab for chi-square was applied to assess the differences in gender and primary kidney disease between the groups. A linear mixed model procedure was used to analyse the difference in the time course of peritoneal solute and fluid transport among the EPS group and both control groups. This test is capable of handling datasets of patients with missing data. The covariance structure between the observations was determined using the AIC criterion on the best fit. Time was included in the model as a covariate.

To study whether the time course of peritoneal function parameters differed between the groups, the interaction term between time and group was added to the model. A significant interaction term indicated a different time course among the groups over time. In absence of a difference in time course, a second analysis was performed; this analysis considered the mean difference in peritoneal function over time among the groups without an interaction term.

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Figure 1| Flow chart of the patient selection for the analysis of the risk of EPS after UFF (left panel, analysis A) and the analysis of the longitudinal data of peritoneal transport parameters (right panel, analysis B).

ResULts

Analysis A: risk of EPS after UFFPatients’ characteristics are given in Table 1. Between July 1995 and December 2008, 417 adult patients were treated with PD in our centre. Of these patients, 224 were treated with PD for more than 2 years; 48 of them developed UFF after at least 24 months and 10 developed EPS (Figure 1, analysis A). EPS patients stayed on PD for a longer period before and after the development of UFF and had a longer total PD duration compared to the controls (p=0.01) Reasons for discontinuation of PD therapy were different between the groups (p=0.01). No statistically significant differences were present for age at onset UFF, co-morbidity, outcome after three years of UFF and causes of death between EPS patients and controls. The interval of the diagnosis of UFF and the development of EPS or discontinuation of PD is given in Table 2. Fifty percent of the patients who stopped PD after more than three years of UFF had EPS or developed it thereafter.

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Table 1| Analysis A: patient characteristic of patients with UFF after 2 years of PD.

Numbers are given in medians and ranges. EPS, encapsulating peritoneal sclerosis; UFF, ultrafiltration failure; PD, peritoneal dialysis.; HD, hemodialysis: TX, kidney transplantation

Chapter 7 Table 1

EPS Control P-value

Number of patients 10 38 Age at time of UFF 36 (22-70) 53 (19-81) 0.07 Total PD duration (months)

92 (53-149) 52 (25-107) <0.01

Interval start PD and development UFF (months)

84 (27-134) 39 (24-100) <0.01

Interval UFF and discontinuation of PD (months)

29 (1-53) 9 (-2-42) 0.02

Interval discontinuation PD and time of death (months)

7.5 (0-47) 0 (0-33) 0.02

Cause of discontinuation PD

0.01

death 1 13 transplantation 0 5 ultrafiltration failure 2 6 EPS 3 - recuring peritonitis 3 6 censoring 0 5 other 1 3 Outcome 3 years after UFF

0.58

death 6 20 PD - 4 HD 3 7 TX 1 7

Causes of death 0.16 cardio vascular 1 3 peritonitis 1 5 Intestinal ischeamia

2 2

pulmonary infection

- 1

voluntary discontinuation

2 3

unknown - 6

Chapter 7 – Table 2

Years of UFF until the discontinuation of PD

0-1 1-2 2-3 >3

EPS 3 1 4 2 Control 22 11 3 2 EPS as proportion of totals with UFF (%) 12 8 57 50

Chapter 7 Table 1

EPS Control P-value

Number of patients 10 38 Age at time of UFF 36 (22-70) 53 (19-81) 0.07 Total PD duration (months)

92 (53-149) 52 (25-107) <0.01

Interval start PD and development UFF (months)

84 (27-134) 39 (24-100) <0.01

Interval UFF and discontinuation of PD (months)

29 (1-53) 9 (-2-42) 0.02

Interval discontinuation PD and time of death (months)

7.5 (0-47) 0 (0-33) 0.02

Cause of discontinuation PD

0.01

death 1 13 transplantation 0 5 ultrafiltration failure 2 6 EPS 3 - recuring peritonitis 3 6 censoring 0 5 other 1 3 Outcome 3 years after UFF

0.58

death 6 20 PD - 4 HD 3 7 TX 1 7

Causes of death 0.16 cardio vascular 1 3 peritonitis 1 5 Intestinal ischeamia

2 2

pulmonary infection

- 1

voluntary discontinuation

2 3

unknown - 6

Chapter 7 – Table 2

Years of UFF until the discontinuation of PD

0-1 1-2 2-3 >3

EPS 3 1 4 2 Control 22 11 3 2 EPS as proportion of totals with UFF (%) 12 8 57 50

Table 2| Analysis A: risk of EPS after years of UFF with continuation of PD.

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Analysis B: longitudinal analysis of peritoneal transportBetween July 1995 and December 2008, we analyzed 59 patients who were treated with PD for more than 55 months. EPS was found in 13 patients, 21 patients had UFF and 26 had normal UF. One of the EPS patients was only treated with PD as a child and was excluded from the risk analysis. Another patient, who was excluded from the previous analysis due to absence of UFF, was included in the analysis of functional parameters. Therefore, we included 12 EPS patients, 21 UFF patients and 26 normal UF patients for this analysis (Figure 1, analysis B). Patient characteristics are given in Table 3. EPS patients were younger and had a longer PD duration in spite of the applied restriction of 55 months. The number of peritonitis episodes and the outcome were not different between the groups.

Table 3| Analysis B: patient characteristics for the analysis of peritoneal function

Numbers are given in medians and ranges. *p<0.05. EPS, encapsulating peritoneal sclerosis; UFF, ultrafiltration failure; UF, ultrafiltration; PD, peritoneal dialysis; HD, hemodialysis; TX, kidney transplantation.

Chapter 7 Table 3

EPS UFF Normal UF

Number of patients 12 21 26 Age (years) 37* (21-73) 54 (22-83) 48 (26-87) Gender (male/female) 7/5 11/11 16/12 PD duration (months) 97* (55/154) 72 (55-106) 6 (55-107) Interval diagnosis EPS and discontinuation of PD (months)

2 (-3 – 33)

Peritonitis (number of episodes)

4 (0-15) 3.5 (0-11) 2.5 (0-12)

Outcome death 7 14 9 HD 5 5 2 PD - 2 6 TX - 2 11

Analysis B: small solute transportFigure 2 shows the time courses of MTAC creatinine and MTAC urate in patients who developed EPS and in both control groups. The time courses of the EPS patients showed an increase until two years prior to EPS and a decrease at one year prior to the diagnosis. The time courses of the EPS and UFF group were different from the time course of the normal UF group (MTAC creatinine p=0.03; MTAC urate p=0.06).

Analysis B: large solute transport Figure 3 shows the time course of the clearances of albumin (Alb), immunoglobulin-G (IgG), alpha-2-macroglobulin (A2M) and the restriction coefficient. The time course of the large solutes showed a tendency to decrease with time on PD, although a statistical significance among the groups was not reached. The restriction coefficient showed an increasing trend for all the three groups, indicating a reduced peritoneal permeability to macromolecules with time on PD.

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Figure 3| Analysis B: linear mixed model estimations (mean and SEM) of the time course of the clearance Alb(left upper panel), clearance of IgG (right upper panel), clearance of A2M (left lower panel) and restriction coefficient (right lower panel) in the EPS group (open circles), UFF group (open squares) and normal UF group (open triangles). The number of patients at each time point is given below the horizontal axis. No differences were present between the groups.

Figure 2| Analysis B: linear mixed model estimations (mean and SEM) of the time course of the MTAC creatinine (left panel) and MTAC urate (right panel) in the EPS group (open circles), UFF group (open squares) and normal UF group (triangles). The number of patients at each time point is given below the horizontal axis. The time courses of the EPS and UFF group were different from the time courses of the normal UF group for the MTAC creatinine (p=0.03) and MTAC urate (p=0.06).

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Analysis B: lymphatic absorption and fluid transport Figure 4 shows the time course of the net UF, TCUF and ELAR. The time course of net UF and TCUF shows a decrease in time for the EPS group. The time courses of the EPS and UFF group were different from the time course of the normal UF group (net UF p=0.02; TCUF p=0.07). The normal UF group had higher values for net UF and TCUF (both p<0.01) than the EPS and UFF group. The time course of the ELAR remained stable during PD. No differences in time course were present between the groups. However, the EPS group and the normal UF group had overall significantly lower values than the UFF group (p=0.03).

Figure 5 shows the time course of solute coupled water transport at 60 min, FWT at 60 min and the contribution of FWT to TCUF. Solute-coupled water transport and FWT showed a linear decrease in patients who developed EPS. Similar time courses were present in both control groups for solute-coupled water transport and FWT. The normal UF group had higher values for solute-coupled water transport (p=0.04) and FWT (p<0.01) and the contribution to FWT (p<0.01) than the EPS and UFF group.

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Figure 4| Analysis B: linear mixed model estimations (mean and SEM) of the time course of the net UF (upper panel), TCUF (middle panel) and the ELAR (lower panel) in the EPS group (open circles), UFF group (open squares) and normal UF group (open triangles). The number of patients at each time point is given below the horizontal axis. The time courses of the EPS and UFF group were significantly different from the time courses of the normal UF group for the net UF (p=0.02) and TCUF (p=0.07). The EPS and UFF group had overall lower values compared to the normal UF group for net UF and TCUF (both p<0.01). The time course of the ELAR was not different between the groups. However, the EPS and normal UF group had overall lower values compared to the UFF group (p=0.03).

Figure 5| Analysis B: linear mixed model estimations (mean and SEM) of the time course of solute-coupled water transport (upper panel), free water transport at 60 min (middle panel) and the contribution of FWT to TCUF (lower panel) in the EPS group (open circles), UFF group open squares) and normal UF group (open triangles). The number of patients at each time point is given below the horizontal axis. The EPS and UFF group had overall lower values compared to the normal UF group for solute-coupled water transport (p=0.06), FWT at 60 minutes (p<0.01) and the contribution of FWT (p<0.01).

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DiscUssiOn

The present study investigated the risk of EPS after UFF and the time course of different peritoneal function parameters prior to the development of EPS. Half of the patients who continued PD for 3 years after the development of UFF, developed EPS. The UFF patients who developed EPS had a longer PD duration and continued PD for a longer period after UFF had developed, when compared to those who did not develop EPS. The association between UFF and EPS has often been described1,2,5,6, but the risk of getting EPS in long-term UFF patients has not been analysed before. The EPS patients had a longer PD duration, developed UFF in later stage and continued PD therapy for a longer period once UFF was present in comparison to control patients. The duration of PD therapy is a risk factor for the development of EPS. Whether this difference between the groups causes the difference in outcome is unknown. Twenty controls patients died, six of these patients died at home without signs of EPS. Two patients died of intestinal ischemia, but the diagnosis of EPS could not be made in them. In this study, one could question the strict definition of UFF with a cut-off value of 400mL. Therefore, an additional analysis was performed with a definition of UFF of < 400mL/4h/3.86% glucose with an intra-individual coefficient of variation of 17% (net ultrafiltration = 470mL/4h/3.86%) 19. Sixty two patients with UFF were included, 12 of them developed EPS. This did not influence the results.

Peritoneal small solute transport showed trends with maximum values at 2 years prior the diagnosis of EPS. Similar trends were seen in controls with UFF. The increase in small solute transport trends may suggest an increasing peritoneal surface area due to neoangiogenesis20. The cause of the decrease in small solute and protein transport 2 years prior to EPS is speculative. It could be due to fibrotic abnormalities in peritoneal interstitial tissue. The increase of fibrotic abnormalities is suggested by the upward slope of the restriction coefficient for proteins. This indicates an increase in size-selective restriction of protein transport. However, the time course of this parameter was similar in all groups. Therefore, this is not the only explanation.

The ELAR is a measure of peritoneal lymphatic drainage through two different pathways, the subdiaphragmatic uptake and transmesothelial transport to interstitial tissues14,16. Both angiogenesis and lymphangiogenesis have been described in the stainings of visceral peritoneum of patients with EPS21. Therefore, an increase in ELAR was expected and the absence of this increase may be explained by a decreased uptake into the subdiaphragmatic lymph vessels or the interstitial tissues. It is speculative whether this is caused by sclerosis or by a malfunction of the subdiaphragmatic stomata.

Solute-coupled water transport, FWT at 60 min and net UF at 240 minutes showed downward linear trends with the development of EPS and UFF. A decrease in net UF during follow-up has been found by us previously 22. The contribution of FWT to TCUF remained stable over time. The decrease in solute-coupled water transport and FWT suggests a role of interstitial fibrosis. An additional effect of aquaporin-1 dysfunction on FWT cannot be excluded 23.

Making an early diagnosis of EPS is difficult. The current study showed that the time course of peritoneal transport parameters cannot distinguish between those with UFF from those who will develop EPS. In a previous study we analysed various effluent markers prior to the development of EPS. The combination of an appearance rate of CA-125 < 33 U/min and an appearance rate of IL-6 > 350 pg/min had a sensitivity of 70% and a specificity of 100% for the development of EPS in patients with UFF. This

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indicates the potential use of a combination of peritoneal transport parameters and effluent markers for an early diagnosis of EPS 24. However, this needs confirmation in other studies on this subject.

A limitation of this study is that, despite the restriction on PD duration of 55 months applied in the control groups, the PD duration was longer in the EPS group. Matching for PD duration was not possible due to the long duration in the EPS group and the division between UFF and normal UF in the control groups. The power of this study is limited due to rarity of EPS. A multi-centre design would improve the power. However, to our knowledge, we are the only centre that regularly assesses the peritoneal membrane function with a 3.86% glucose dwell in combination with a volume marker. Some of the results of this study can also be measured with a regular PET. The fast transport status can be assessed with dialysate over plasma ratios of creatinine. For the diagnosis of UFF the 2.27% glucose dwell should be replaced by a 3.86% dwell. FWT and solute-coupled water transport can be measured by draining the total peritoneal cavity at 60 min and measuring the UF volume. The volume should then be re-infused immediately 25. However, the ELAR can only be measured with the addition of a volume marker.

In conclusion, the risk of EPS increases with the continuation of PD while UFF is present. However, EPS patients show similar small transport characteristics compared to UFF patients. Besides, they show a tendency to a decrease in peritoneal protein clearances. A constantly low ELAR may distinguish the EPS patients from the UFF patients. It should be considered to discontinue PD within 1-2 years after the development of UFF or take other preventive measures especially when UFF is accompanied with a low or decreasing ELAR.

AcKnOWLeDGeMents

This study was supported by a grant from The Dutch Kidney Foundation (Nierstichting) grant: C06.2186

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