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NDT Advance Access originally published online on March 22, 2006
Nephrology Dialysis Transplantation 2006 21(6):1675-1681; doi:10.1093/ndt/gfl054
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© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Original Articles: Dialysis and Transplantation

Quantitative assessment of the peritoneal vessel density and vasculopathy in CAPD patients

Ali M. Sherif1, Masaaki Nakayama2, Yukio Maruyama1, Hiraku Yoshida1, Hiroyasu Yamamoto1, Keitaro Yokoyama1 and Makio Kawakami3

1 Department of Kidney and Hypertension, The Jikei University School of Medicine, Tokyo, 2 Research Division of Dialysis and Chronic Kidney Disease, Tohoku University Graduate School of Medicine, Sendai and 3 Department of Pathology, The Jikei University Hospital, Tokyo, Japan

Correspondence and offprint requests to: Ali M. Sherif, Department of Kidney and Hypertension, The Jikei University School of Medicine, 3-19-18 Nishi shinbashi, Minato ku, Tokyo 105-8471, Japan. Email: alimsherif{at}yahoo.com



   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Background. Peritoneal sclerosis (PS) complicates continuous ambulatory peritoneal dialysis (CAPD). Exploring the peritoneal vascular changes, which are characteristic histological findings in long-term PD, may give new insight into the basic pathological process leading to PS. We present a quantitative analysis of peritoneal vascular density as well as vasculopathy grades in relation to PD duration.

Methods. Peritoneal samples from 56 stable CAPD patients were analysed, and cases with membrane failure were excluded. Patients were classified into four groups according to CAPD duration in years: group A (n = 12), 0 year; group B (n = 11), 1–5 years; group C (n = 17), 5–9 years; and group D (n = 16), >9 years. The total density, of microvessels (capillaries, post-capillary venules and venules) and the density of each vasculopathy grade (0 = intact, 1 = mild, 2 = moderate and 3 = severe) in the compact zone were calculated (numbers/mm2) in each sample and the percentage ratio of each grade in relation to the total vessel density was also determined.

Results. There was no significant difference in the total vessel density (P-value = 0.64). In the grade of vasculopathy (density and percentage ratio), there were significant differences among groups, with grade 0 highest in group A, grade 1 highest in group C and grade 3 highest in group D.

Conclusion. The results of this study indicate that vascular density does not increase, at least in stable uncomplicated PD, and that intact vessels decrease with time on PD, while the severe grades of vasculopathy predominate especially on a long-term basis.

Keywords: peritoneal dialysis; peritoneal membrane; vasculopathy



   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Peritoneal sclerosis (PS) is a pathological problem that develops during continuous ambulatory peritoneal dialysis (CAPD). Histologically, it is characterized by mesothelial loss, thickening of submesothelial connective tissue zone (compact zone) and vascular alterations [1]. Vasculopathy and angiogenesis are reported as the most characteristic features in PD-related peritoneal pathology [1,2].

Anatomically, the peritoneal vascular networks are mainly composed of arterioles, capillaries, post-capillary venules and venules that are embedded in the compact zone. After the start of PD therapy, it is reported that the peritoneal blood vessels undergo either adaptive or pathological changes in both structure and number [3–9], including fibrosis and hyalinization of the vascular media [10], irregular thickening and reduplication of the capillary basement membrane [5], luminal obliteration and an increase of blood vessel density [2].

However, the morphometrical data concerning the vascular density of the diseased vessels are limited, and it remains unclear in regard to their quantitative changes. Exploring this issue may give a new insight to understand the basic pathological process leading to PS.

This study presents a quantitative analysis of the vascular density as well as vasculopathy grades of the peritoneum in relation to PD duration.



   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Patients
Fifty-six Japanese end stage renal disease (ESRD) patients in the PD unit at The Jikei University School of Medicine (Tokyo, Japan), during the period between October 1986 and January 2003, were subjected to this study after giving informed consent, and after approval of the local ethics committee. The group consisted of 31 males (55.4%) and 25 females (44.6%) with a mean age of 53±14 years. The causes of ESRD in those patients were: diabetic nephropathy in four cases (7.1%), biopsy-proven chronic glomerulonephritis in 32 (57.1%), polycystic kidney disease in 5 (8.8%) and unknown in 14 (25.0%). Nephrosclerosis was suspected in most cases of unknown cause, as none of those patients had a history of systemic diseases such as chronic infections, amyloidosis, malignancies or immunological disorders including lupus or vasculitis. Except for 12 new PD cases, all the patients had been treated by PD for periods ranging between 12 and 179 months (mean = 70.55±54.43 months) using conventional glucose-based PD fluid (Dianeal PD-2/4; Baxter Ltd, Tokyo, Japan) in a regimen of 4–5 exchanges per day. The patients who had experienced peritonitis within 6 months prior to this investigation, and cases with membrane failure or where encapsulating peritoneal sclerosis (EPS) was suspected, were not included in this study.

The patients were classified into four groups according to the duration on PD as follows: group A, 12 patients who had just started PD; group B, 11 patients who had been treated with CAPD for periods between 1 and 5 years; group C, 17 patients who had been treated with CAPD for periods between 5 and 9 years and group D, 16 patients who had been treated with CAPD for periods more than 9 years. The patients of the four groups were well-matched regarding their age, sex and underlying renal diseases (Table 1).


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  		Table 1. Patients’ demographic data

 
Peritoneal biopsy
Peritoneal samples were collected at the time of insertion (n = 12), exchange (n = 25) of Tenckhoff catheters or PD withdrawal (n = 19). The reasons for exchanges were catheter malfunction in 12 cases and subcutaneous tunnel infection in 13 cases. The reasons for PD withdrawal were inadequate fluid balance due to excess salt intake in five cases, inadequate dialysis in six cases, patient's preference in five cases and other reasons in three cases. The samples were taken at least 5 cm away from the site of the original catheter insertion. The peritoneal samples were immediately fixed in formalin solution and stained with Haematoxylin and Eosin, modified Masson-Noguchi, periodic acid Schiff and elastic van Gieson stains. All the samples were examined in the Pathology Department of The Jikei University School of Medicine by an experienced histopathologist, who was blinded to patient characteristics and clinical details, using Olympus light microscope, Zeiss AxioCam camera and Axiovision 3.1 Windows computer software program, as described subsequently.

Histological analysis
Vascular density
In each sample, the submesothelial compact zone was identified as the membrane area extending from the surface mesothelium down to the upper limit of the fatty tissue, the surface area of the compact zone in square millimetres and peritoneal surface length examined in millimetres was measured using Axiovision Windows software for morphometrical measurements. Regarding the size of the samples, only compact zones with more than 0.3 mm2 surface area were subjected to analysis. The total number of sectioned blood vessels (capillaries, post-capillary venules and venules) within the compact zone was counted, and then this number was divided by total compact zone area (mm2) and mesothelial surface length (mm).

Grading of vasculopathy
All the capillaries, post-capillary venules and venules within the compact zone were identified by a light microscope to give the grading of vasculopathy. The clearest determination was acheived using Masson-Noguchi staining, as previously reported, and as demonstrated by the findings of monolayer structures consisting of endothelial cells without smooth muscle cells [11]. The grade was assigned according to the definition by Honda et al. [12] as follows: grade 0 (intact), no vascular abnormality; grade 1, mild peri-vascular fibrosis without narrowing of the lumen; grade 2, moderate peri-vascular fibrosis and thickening of the vascular wall with mild to moderate narrowing of the lumen with grade 3, severe peri-vascular fibrosis with marked narrowing or occlusion of the lumen (Figure 1A–D). The density of each vasculopathy grade was calculated in each sample and the percentage ratio of the mean value of each grade in relation to the mean value of total vessel density was also determined.


Figure 1
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  		Fig. 1. Grading of peritoneal vasculopathy. (A) Peritoneal blood vessels with grade 0 vasculopathy (Masson-Noguchi stain): No vascular abnormality; (B) Peritoneal blood vessels with grade 1 vasculopathy (Masson-Noguchi stain): mild peri-vascular fibrosis without narrowing of the lumen; (C) Peritoneal blood vessels with grade 2 vasculopathy (Masson-Noguchi stain): Moderate peri-vascular fibrosis and thickening of the vascular wall with mild to moderate narrowing of the lumen; and (D) Peritoneal blood vessels with grade 3 vasculopathy (Masson-Noguchi stain): Severe peri-vascular fibrosis and marked narrowing or occlusion of the lumen.

 
Measurement of compact zone thickness
The maximum and minimum thicknesses of the compact zone was measured in micrometres (µm), then the median value of both measurements was recorded.

Peritoneal equilibration test
The dialysate to plasma (D/P) creatinine values of the peritoneal equilibration test (PET) results were obtained 2 months after the catheter insertion or within 2 months before catheter exchange or removal.

Statistical analysis
Data are presented as mean±SD. A P-value of less than 0.05 was considered to be statistically significant. Differences between the four groups were analysed using the one-way analysis of variance (ANOVA). The Tukey–Kramer test was used to determine which group caused the difference. Nominal variables were tested using chi-square test. Statistical analyses were performed using JMP, version 5.1.1 for Windows (SAS Institute Inc., Cary, NC, USA).



   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
Histological analysis
There were no significant differences in the total vascular density (number/mm2: compact zone) (26.6±15.4, 37.2±21.5, 36.6±21.7 and 34.7±24.9 for group A, B, C and D, respectively) (P = 0.59, Figure 2). Moreover, there were no significant differences regarding the total number of vessels per surface membrane length in µm (5.5±1.3, 9.6±2.3, 27.4±32.6 and 10.5±7.2 for groups A–D, respectively; P = 0.12). Table 2 shows the vasculopathy density (number/mm2: compact zone of each group). There was no significant change in the density of grade 0 (intact) blood vessels among the four groups (P = 0.07). The density of grade 1 (mild) vasculopathy showed significant difference (P = 0.02) with significances in group C vs A. The density of grade 2 (moderate) vasculopathy did not reach stastical significance (P = 0.10). The density of grade 3 (severe) vasculopathy showed a significant difference (P = 0.03) compared with significances in group D vs A and C.


Figure 2
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  		Fig. 2. Total blood vessel density (number/mm2: compact zone area) and CAPD duration. The total number of sectioned blood vessels (capillaries, post-capillary venules and venules) within the compact zone were measured in each case. No significant differences were found among the four groups (P = 0.59). Group A: patients before commencement of CAPD (n = 12); group B: patients on CAPD for 1–5 years (n = 11); group C: patients on CAPD for 5–9 years (n = 17); and group D: patients on CAPD for more than 9 years (n = 16).

 

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  		Table 2. Vessel density (number/mm2: compact zone area) with respect to vasculopathy grade by CAPD duration

 
Figure 3 (A–D) represents the percentage ratio of the density of each grade of vasculopathy in relation to the total vascular density among the four groups. The mean percentage of grade 0 showed a significant difference (76.0, 51.5, 34.5 and 28.1%, respectively; P<0.01) compared with significances in group A vs C and D. The mean percentage of grade 1 showed a significant difference (17.4, 24.0, 44.2 and 27.2%, respectively; P = 0.01) compared with significances in group C vs A, B and D. The mean percentage of grade 2 showed no significant difference (3.2, 8.6, 10.5 and 10.2%, respectively; P = 0.11). The mean percentage of grade 3 showed a significant difference (0.0, 15.9, 10.8 and 34.5%, respectively; P = 0.04) compared with significances in group D vs A, B and C. For compact zone thickness, the mean thickness of compact zone in each group was as follows: 141.67±35.47 µm in group A, 235.83±138.17 µm in group B, 505.65±345.04 µm in group C and 353.08±271.59 µm in group D, respectively. Significance was demonstrate between group A and the other three groups (P = 0.02); however, no significant differences were found among the three PD groups (P = 0.08).


Figure 3
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  		Fig. 3. Changes in the ratio of the each grade of vasculopathy to the total blood vessel number with CAPD duration among the 4 groups: The numbers of the blood vessels of each grade of vasculopathy were measured then divided over the number of total sectioned blood vessels (capillaries, post-capillary venule and venule) within the compact zone. (A) Grade 0 vasculopathy. There is a significance in the mean values among 4 groups (P<0.01). * Group A vs C and group A vs D. (B) Grade 1 vasculopathy. There is a significance in the mean values among 4 groups (P<0.01). * Group C vs A; group C vs B and group C vs D. (C) Grade 2 vasculopathy. No significant differences are found among 4 groups (P = 0.10). (D) Grade 3 vasculopathy. There is a significance in the mean values among 4 groups (P = 0.04). * Group D vs A; Group D vs B and Group D vs C. Group A: patients before commencement of CAPD (n = 12). Group B: patients on CAPD with 1 to 5 years (n = 11), Group C: patients on CAPD with 5 to 9 years (n = 17) and Group D: patients on CAPD with more than 9 years (n = 16). The "*" sign means: Significance in.

 
PET
The D/P creatinine values of the PET were obtained from 48 patients (8 from group A, 10 from group B, 15 from group C and 15 from group D). The data were as follows: 0.63±0.08 in group A, 0.71±0.11 in group B, 0.72±0.15 in group C and 0.77±0.10 in group D. A significant difference in the D/P creatinine values (P = 0.03) was noticed.



   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
The aim of this study is to give a quantitative analysis on the vascular density as well as the vasculopathy grades of peritoneum in relation to PD duration, in order to understand the basic pathological process of peritoneal injury by PD treatment. In this study, we present two special categories of PD patients: the non-dialysed ESRD cases at 0 month (group A) and the long-term PD patients treated for more than 9 years (group D) in addition to two other groups, the early term PD patients treated for 1–5 years duration (group B) and the mid-term cases treated for 5–9 years duration (group C). Patients who had a history of peritonitis 6 months before the peritoneal biopsy and cases with membrane failure or suspected EPS were not included in this study. All patients had been on PD and had never been treated by haemodialysis in the past except those in group A. Therefore, those peritoneal samples could well reflect the impact of PD treatment.

The measurement method employed here was different from the previously reported ones [1,2]. The methodology for morphometrical analysis differed between studies. In vascular density, there are two different methods reported; ‘vessel number per microscopic field’ by Mateijsen et al. [2], and ‘vessel number per length of surface peritoneum’ by Williams et al. [1]. To evaluate as objectively as possible, all the sectioned blood vessels within the submesothelial fibrous layer—compact zone, were determined and counted (total vessel number per compact zone area in square millimetre). We believe this analysis could be objectively applied in studying membranes with different thickness and length.

The role of angiogenesis for the primary pathophysiology in PD peritoneal injury has been suggested, and this concept has been verified [13]. However, in this study, the total vascular density in relation to surface area showed no significant differences among groups. In addition, no significant differences were found in vascular density among PD groups (B, C and D). Furthermore, the thickness of the compact zone among them did not show any significant differences, while the thickness of the compact zone was significantly thinner in pre-PD patients (group A) when compared with PD groups (P = 0.02). This may indicate that the process of peritoneal vascular proliferation progresses in coordination with the extent of fibrosis or expansion of compact zone mass. On the other hand, the data on vessel number per surface membrane length showed no significance in relation to CAPD duration; however, the date seem to indicate a trend towards differences between the groups as demonstrated by the individual variance in range in groups A and B and the relatively low P-value obtained (P = 0.12). This may suggest a type 2 error and it is supposed that a larger material would have shown a significant difference concerning this variable (a limitation in our study).

In regard to the reason for the controversial findings on peritoneal vessel densities, we presume that the development of angiogenic response is closely related to the basal inflammatory state of the membrane, as in patients with severe membrane failure or sclerosing peritonitis as reported by previous studies [1,2]. In our study, such patients were all excluded.

Vasculopathy, defined as fibrous thickening and sclerosis of the vessel wall with various degrees of luminal obliteration that dominantly involves the post-capillary systems of peritoneum in PD [1,2,12,14,15]. The methodology of assigning the vasculopathy grade according to the worst lesion of the specimen, showed that the progression of vasculopathy is one of the characteristic findings in long-term PD patients [1]. In this study, we aimed to relate the complete findings concerning the diseased vessels of peritoneum. With respect to vasculopathy density grades, there were significant differences in grade 0, 1 as well as 3 and nearly significant differences in grade 2. This suggests that the PD duration has an impact on the progression of vasculopathy. In fact, the percentage ratio of vasculopathy grades clearly supports this premise; the highest values of grade 0 were in group A, grade 1 of in group C and grade 3 of in group D. This may indicate a decline of the intact vessels and a progression of vasculopathy with prolongation of PD (Figure 3).

However, the pathological process is not absolutely uniform and the reality of peritoneal pathology presented various degrees of vasculopathy, including intact vessels, even in the cases having severe lesions. This observation may indicate that the most severe lesion does not necessarily represent the dominant findings of the sample. This opens a discussion on how to estimate vasculopathy grading. In this study, increases of total vascular density in accordance with PD duration were not found. Moreover, the prevalence of severe vasculopathy was dominated by loss of intact vessels in the long-term PD group. When taking those two observations into account, it could be hypothesized that the process of increased vascular mass occurs in coordination with increased compact zone mass, and where as the excess angiogenesis is not a common finding, the primary pathological process of peritoneal vasculatures in relation time on PD, is the progression of pathological changes and loss of intact vessels.

Increased solute transport is a risk factor for patient prognosis [16–21] and development of EPS [22–24]. Animal studies indicated the critical role of angiogenesis in the peritoneal membrane for the increased solute transport. Vascular endothelial growth factor (VEGF), a potent angiogenic factor, leads to an increase of vascular density and creatinine transport of the membrane [25], whereas overexpression of angiostatin reduces PD-mediated new vessel formation and restores loss of ultrafiltration [26]. However, this phenomenon was not clearly demonstrated in this study, despite the fact that the D/P creatinine ratio tended to increase in accordance to the duration of PD in our study. Among the patients available for PET data, we did not find any significant correlations between D/P creatinine and compact zone thickness, vascular density of compact zone area or vascular number per peritoneal surface length (data not shown). It is not well determined if there is a close correlation between the pathological results of this study and the significant increase of transport state with PD duration. Factor(s) other than increased vascular density or mass may play a critical role in the increased membrane transport state. Whether the progression of vasculopathy could be involved in this pathology is an issue to be clarified in future.

In conclusion, the results of this study indicate that vascular density does not increase, at least in stable uncomplicated PD, while intact vessels decrease with time on PD and the severe grades of vasculopathy predominate, especially on a long-term basis.



   Acknowledgments
 
The author thanks Prof. Tatsue Hosoya, MD, Head of the Department of Kidney and Hypertension, The Jikei University School of Medicine, Tokyo, Japan for his help and appreciates his support. We also thank Professor Yoshindo Kawaguchi, MD, The Jikei University School of Medicine, Tokyo, Japan for his valuable suggestions and advice.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. Williams JD, Craig KJ, Topley N et al. Peritoneal Biopsy Study Group. Morphologic changes in the peritoneal membrane of patients with renal disease. J Am Soc Nephrol 2002; 13: 470–479[Abstract/Free Full Text]
  2. Mateijsen MA, van der Wal AC, Hendriks PM et al. Vascular and interstitial changes in the peritoneum of CAPD patients with peritoneal sclerosis. Perit Dial Int 1999; 19: 517–525[Abstract/Free Full Text]
  3. Dobbie J, Zaki M, Wilson L. Ultrastructural studies on the peritoneum with special reference to chronic ambulatory peritoneal dialysis. Scott Med J 1981; 26: 213–223[Web of Science][Medline]
  4. Dobbie JW. Morphology of the peritoneum in CAPD. Blood Purif 1989; 7: 74–85[Web of Science][Medline]
  5. Pollock CA, Ibels LS, Eckstein RP et al. Peritoneal morphology on maintenance dialysis. Am J Nephrol 1989; 9: 198–204[Web of Science][Medline]
  6. Rubin J, Rogers WA, Taylor HM, Everett D, Provant B, Nolph KD. Peritonitis during continuous ambulatory peritoneal dialysis. Ann Intern Med 1980; 92: 7–13[Abstract/Free Full Text]
  7. Gotloib L, Shostack A. Ultrastructural morphology of the peritoneum: new findings and speculations on transfer of solutes and water during peritoneal dialysis. Perit Dial Bull 1987; 7: 119–129
  8. Di Paolo N, Sacchi G, De Mia M et al. Morphology of the peritoneal membrane during continuous ambulatory peritoneal dialysis. Nephron 1986; 44: 204–211[Web of Science][Medline]
  9. Di Paolo N, Sacchi G, Buoncristiani V. The morphology of the human peritoneum in CAPD patients. In: Maher J, ed. Frontiers in Peritoneal Dialysis. Field Rich, New York; 1985: 11–19
  10. Slingeneyer A, Canaud B, Mion C. Permanent loss of ultrafiltration capacity of the peritoneum in long-term peritoneal dialysis: an epidemiological study. Nephron 1983; 33: 133–138[Medline]
  11. Numata M, Nakayama M, Nimura S, Kawakami M, Lindholm B, Kawaguchi Y. Association between an increased surface area of peritoneal microvessels and a high peritoneal solute transport rate. Perit Dial Int 2003; 23: 116–122[Abstract/Free Full Text]
  12. Honda K, Nitta K, Horita S et al. Accumulation of advanced glycation end products in the peritoneal vasculature of continuous ambulatory peritoneal dialysis patients with low ultra-filtration. Nephrol Dial Transplant 1999; 14: 1541–1549[Abstract/Free Full Text]
  13. Devuyst O. New insights in the molecular mechanisms regulating peritoneal permeability. Nephrol Dial Transplant 2002; 17: 548–551[Free Full Text]
  14. Gotloib L, Shostack A. Ultrastructural morphology of the peritoneum: new findings and speculations on transfer of solutes and water during peritoneal dialysis. Perit Dial Bull 1987; 7: 119–129
  15. Zweers MM, de Waart DR, Smit W, Struijk DG, Krediet RT. Growth factors VEGF and TGF-beta1 in peritoneal dialysis. J Lab Clin Med 1999; 134: 124–132[CrossRef][Web of Science][Medline]
  16. Kawaguchi Y, Hasegawa T, Nakayama M, Kubo H, Shigematu T. Issues affecting the longevity of the continuous peritoneal dialysis therapy. Kidney Int Suppl 1997; 62: S105–S107[Medline]
  17. Heaf J. CAPD adequacy and dialysis morbidity: detrimental effect of a high peritoneal equilibration rate. Ren Fail 1995; 17: 575–587[Medline]
  18. Davies SJ, Phillips L, Russell GI. Peritoneal solute transport predicts survival on CAPD independently of residual renal function. Nephrol Dial Transplant 1998; 13: 962–968[Abstract/Free Full Text]
  19. Wu CH, Huang CC, Huang JY, Wu MS, Leu ML. High flux peritoneal membrane is a risk factor in survival of CAPD treatment. Adv Perit Dial 1996; 12: 105–109[Medline]
  20. Wang T, Heimburger O, Waniewski J, Bergstrom J, Lindholm B. Increased peritoneal permeability is associated with decreased fluid and small-solute removal and higher mortality in CAPD patients. Nephrol Dial Transplant 1998; 13: 1242–1249[Abstract/Free Full Text]
  21. Chung SH, Chu WS, Lee HA et al. Peritoneal transport characteristics, comorbid diseases and survival in CAPD patients. Perit Dial Int 2000; 20: 541–547[Abstract/Free Full Text]
  22. Yamamoto R, Otsuka Y, Nakayama M et al. Risk factors for encapsulating peritoneal sclerosis in patients who have experienced peritoneal dialysis treatment. Clin Exp Nephrol 2005; 9: 148–152[Medline]
  23. Yamamoto R, Nakayama M, Hasegawa T et al. High-transport membrane is a risk factor for encapsulating peritoneal sclerosis developing after long-term continuous ambulatory peritoneal dialysis treatment. Adv Perit Dial 2002; 18: 131–134[Medline]
  24. Nakayama M, Ikeda M, Katoh N et al. Long-standing high-transport membrane as a risk factor for EPS development after PD withdrawal: an analysis based on changes in peritoneal function during and after CAPD withdrawal. Nippon Jinzo Gakkai Shi 2002; 44: 396–401[Medline]
  25. De Vriese AS, Tilton RG, Stephan CC, Lameire NH. Vascular endothelial growth factor is essential for hyperglycemia-induced structural and functional alterations of the peritoneal membrane. J Am Soc Nephrol 2001; 12: 1734–1741[Abstract/Free Full Text]
  26. Margetts PJ, Gyorffy S, Kolb M, Yu L, Hoff CM, Holmes CJ, Gauldie J. Antiangiogenic and antifibrotic gene therapy in a chronic infusion model of peritoneal dialysis in rats. J Am Soc Nephrol 2002; 13: 721–728[Abstract/Free Full Text]
Received for publication: 18. 9.05
Accepted in revised form: 31. 1.06


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