Low-GDP, pH-neutral solutions preserve peritoneal endothelial glycocalyx during long-term peritoneal dialysis.
Adult
Aged
Biopsy
Capillaries
/ metabolism
Dialysis Solutions
/ adverse effects
Endothelial Cells
/ metabolism
Female
Glucose
/ metabolism
Glycocalyx
/ metabolism
Heparitin Sulfate
/ metabolism
Humans
Hydrogen-Ion Concentration
Male
Middle Aged
Peritoneal Dialysis
Peritoneum
/ blood supply
Plant Lectins
/ metabolism
Platelet Endothelial Cell Adhesion Molecule-1
/ metabolism
Acidic
Endothelial glycocalyx
Peritoneal dialysis
Postcapillary venule
Vasculopathy
pH-neutral
Journal
Clinical and experimental nephrology
ISSN: 1437-7799
Titre abrégé: Clin Exp Nephrol
Pays: Japan
ID NLM: 9709923
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
22
02
2021
accepted:
12
05
2021
pubmed:
18
5
2021
medline:
12
1
2022
entrez:
17
5
2021
Statut:
ppublish
Résumé
During peritoneal dialysis (PD), solute transport and ultrafiltration are mainly achieved by the peritoneal blood vasculature. Glycocalyx lies on the surface of endothelial cells and plays a role in vascular permeability. Low-glucose degradation product (GDP), pH-neutral PD solutions reportedly offer higher biocompatibility and lead to less peritoneal injury. However, the effects on the vasculature have not been clarified. Peritoneal tissues from 11 patients treated with conventional acidic solutions (acidic group) and 11 patients treated with low-GDP, pH-neutral solutions (neutral group) were examined. Control tissues were acquired from 5 healthy donors of kidney transplants (control group). CD31 and ratio of luminal diameter to vessel diameter (L/V ratio) were evaluated to identify endothelial cells and vasculopathy, respectively. Immunostaining for heparan sulfate (HS) domains and Ulex europaeus agglutinin-1 (UEA-1) binding was performed to assess sulfated glycosaminoglycans and the fucose-containing sugar chain of glycocalyx. Compared with the acidic group, the neutral group showed higher CD31 positivity. L/V ratio was significantly higher in the neutral group, suggesting less progression of vasculopathy. Both HS expression and UEA-1 binding were higher in the neutral group, whereas HS expression was markedly more preserved than UEA-1 binding in the acidic group. In vessels with low L/V ratio, which were found only in the acidic group, HS expression and UEA-1 binding were diminished, suggesting a loss of glycocalyx. Peritoneal endothelial glycocalyx was more preserved in patients treated with low-GDP, pH-neutral solution. The use of low-GDP, pH-neutral solutions could help to protect peritoneal vascular structures and functions.
Sections du résumé
BACKGROUND
BACKGROUND
During peritoneal dialysis (PD), solute transport and ultrafiltration are mainly achieved by the peritoneal blood vasculature. Glycocalyx lies on the surface of endothelial cells and plays a role in vascular permeability. Low-glucose degradation product (GDP), pH-neutral PD solutions reportedly offer higher biocompatibility and lead to less peritoneal injury. However, the effects on the vasculature have not been clarified.
METHODS
METHODS
Peritoneal tissues from 11 patients treated with conventional acidic solutions (acidic group) and 11 patients treated with low-GDP, pH-neutral solutions (neutral group) were examined. Control tissues were acquired from 5 healthy donors of kidney transplants (control group). CD31 and ratio of luminal diameter to vessel diameter (L/V ratio) were evaluated to identify endothelial cells and vasculopathy, respectively. Immunostaining for heparan sulfate (HS) domains and Ulex europaeus agglutinin-1 (UEA-1) binding was performed to assess sulfated glycosaminoglycans and the fucose-containing sugar chain of glycocalyx.
RESULTS
RESULTS
Compared with the acidic group, the neutral group showed higher CD31 positivity. L/V ratio was significantly higher in the neutral group, suggesting less progression of vasculopathy. Both HS expression and UEA-1 binding were higher in the neutral group, whereas HS expression was markedly more preserved than UEA-1 binding in the acidic group. In vessels with low L/V ratio, which were found only in the acidic group, HS expression and UEA-1 binding were diminished, suggesting a loss of glycocalyx.
CONCLUSION
CONCLUSIONS
Peritoneal endothelial glycocalyx was more preserved in patients treated with low-GDP, pH-neutral solution. The use of low-GDP, pH-neutral solutions could help to protect peritoneal vascular structures and functions.
Identifiants
pubmed: 33999275
doi: 10.1007/s10157-021-02078-9
pii: 10.1007/s10157-021-02078-9
doi:
Substances chimiques
Dialysis Solutions
0
PECAM1 protein, human
0
Plant Lectins
0
Platelet Endothelial Cell Adhesion Molecule-1
0
Ulex europaeus lectins
0
Heparitin Sulfate
9050-30-0
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1035-1046Subventions
Organisme : Ministry of Education
ID : 18K08258
Informations de copyright
© 2021. Japanese Society of Nephrology.
Références
Krediet RT, Lindholm B, Rippe B. Pathophysiology of peritoneal membrane failure. Perit Dial Int. 2000;20(4_suppl):22–42.
doi: 10.1177/089686080002004S03
Garcia-Lopez E, Lindholm B, Davies S. An update on peritoneal dialysis solutions. Nat Rev Nephrol. 2012;8(4):224–33.
pubmed: 22349485
doi: 10.1038/nrneph.2012.13
Devuyst O, Margetts PJ, Topley N. The pathophysiology of the peritoneal membrane. J Am Soc Nephrol. 2010;21(7):1077–85.
pubmed: 20448020
doi: 10.1681/ASN.2009070694
Perl J, Nessim SJ, Bargman JM. The biocompatibility of neutral pH, low-GDP peritoneal dialysis solutions: benefit at bench, bedside, or both? Kidney Int. 2011;79(8):814–24.
pubmed: 21248712
doi: 10.1038/ki.2010.515
Yohanna S, Alkatheeri AM, Brimble SK, McCormick B, Iansavitchous A, Blake PG, et al. Effect of neutral-pH, low-glucose degradation product peritoneal dialysis solutions on residual renal function, urine volume, and ultrafiltration: a systematic review and meta-analysis. Clin J Am Soc Nephrol. 2015;10(8):1380–8.
pubmed: 26048890
pmcid: 4527022
doi: 10.2215/CJN.05410514
Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch. 2000;440(5):653–66.
pubmed: 11007304
doi: 10.1007/s004240000307
Butler MJ, Down CJ, Foster RR, Satchell SC. The pathological relevance of increased endothelial glycocalyx permeability. Am J Pathol. 2020;190(4):742–51.
pubmed: 32035881
pmcid: 7163249
doi: 10.1016/j.ajpath.2019.11.015
Liu HQ, Li J, Xuan CL, Ma HC. A review on the physiological and pathophysiological role of endothelial glycocalyx. J Biochem Mol Toxicol. 2020;34:e22571.
pubmed: 32659867
Ushiyama A, Kataoka H, Iijima T. Glycocalyx and its involvement in clinical pathophysiologies. J Intensive Care. 2016;4(1):59.
pubmed: 27617097
pmcid: 5017018
doi: 10.1186/s40560-016-0182-z
Flessner MF. Endothelial glycocalyx and the peritoneal barrier. Perit Dial Int. 2008;28(1):6–12.
pubmed: 18178940
doi: 10.1177/089686080802800102
Henry CB, Duling BR. TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol. 2000;279(6):H2815–23.
pubmed: 11087236
doi: 10.1152/ajpheart.2000.279.6.H2815
Matsuki T, Duling BR. TNF-alpha modulates arteriolar reactivity secondary to a change in intimal permeability. Microcirculation. 2000;7(6 Pt 1):411–8.
pubmed: 11142338
doi: 10.1111/j.1549-8719.2000.tb00139.x
Rubio-Gayosso I, Platts SH, Duling BR. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. 2006;290(6):H2247–56.
pubmed: 16399871
doi: 10.1152/ajpheart.00796.2005
Nieuwdorp M, van Haeften TW, Gouverneur MC, Mooij HL, van Lieshout MH, Levi M, et al. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes. 2006;55(2):480–6.
pubmed: 16443784
doi: 10.2337/diabetes.55.02.06.db05-1103
Zuurbier CJ, Demirci C, Koeman A, Vink H, Ince C. Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells. J Appl Physiol. 2005;99(4):1471–6.
pubmed: 16024521
doi: 10.1152/japplphysiol.00436.2005
Tawada M, Hamada C, Suzuki Y, Sakata F, Sun T, Kinashi H, et al. Effects of long-term treatment with low-GDP, pH-neutral solutions on peritoneal membranes in peritoneal dialysis patients. Clin Exp Nephrol. 2019;23(5):689–99.
pubmed: 30547267
doi: 10.1007/s10157-018-1679-7
Kawanishi K, Honda K, Tsukada M, Oda H, Nitta K. Neutral solution low in glucose degradation products is associated with less peritoneal fibrosis and vascular sclerosis in patients receiving peritoneal dialysis. Perit Dial Int. 2013;33(3):242–51.
pubmed: 23123670
pmcid: 3649892
doi: 10.3747/pdi.2011.00270
Schaefer B, Bartosova M, Macher-Goeppinger S, Sallay P, Voros P, Ranchin B, et al. Neutral pH and low-glucose degradation product dialysis fluids induce major early alterations of the peritoneal membrane in children on peritoneal dialysis. Kidney Int. 2018;94(2):419–29.
pubmed: 29776755
doi: 10.1016/j.kint.2018.02.022
Kinashi H, Ito Y, Mizuno M, Suzuki Y, Terabayashi T, Nagura F, et al. TGF-beta1 promotes lymphangiogenesis during peritoneal fibrosis. J Am Soc Nephrol. 2013;24(10):1627–42.
pubmed: 23990681
pmcid: 3785267
doi: 10.1681/ASN.2012030226
Sawai A, Ito Y, Mizuno M, Suzuki Y, Toda S, Ito I, et al. Peritoneal macrophage infiltration is correlated with baseline peritoneal solute transport rate in peritoneal dialysis patients. Nephrol Dial Transpl. 2011;26(7):2322–32.
doi: 10.1093/ndt/gfq702
Tawada M, Ito Y, Hamada C, Honda K, Mizuno M, Suzuki Y, et al. Vascular endothelial cell injury is an important factor in the development of encapsulating peritoneal sclerosis in long-term peritoneal dialysis patients. PLoS ONE. 2016;11(4):e0154644.
pubmed: 27119341
pmcid: 4847858
doi: 10.1371/journal.pone.0154644
Ten Dam GB, Kurup S, van de Westerlo EM, Versteeg EM, Lindahl U, Spillmann D, et al. 3-O-sulfated oligosaccharide structures are recognized by anti-heparan sulfate antibody HS4C3. J Biol Chem. 2006;281(8):4654–62.
pubmed: 16373349
doi: 10.1074/jbc.M506357200
Kurup S, Wijnhoven TJ, Jenniskens GJ, Kimata K, Habuchi H, Li JP, et al. Characterization of anti-heparan sulfate phage display antibodies AO4B08 and HS4E4. J Biol Chem. 2007;282(29):21032–42.
pubmed: 17517889
doi: 10.1074/jbc.M702073200
Ravida A, Musante L, Kreivi M, Miinalainen I, Byrne B, Saraswat M, et al. Glycosylation patterns of kidney proteins differ in rat diabetic nephropathy. Kidney Int. 2015;87(5):963–74.
pubmed: 25587705
doi: 10.1038/ki.2014.387
Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 2007;454(3):345–59.
pubmed: 17256154
pmcid: 1915585
doi: 10.1007/s00424-007-0212-8
Thompson SM, Fernig DG, Jesudason EC, Losty PD, van de Westerlo EM, van Kuppevelt TH, et al. Heparan sulfate phage display antibodies identify distinct epitopes with complex binding characteristics: insights into protein binding specificities. J Biol Chem. 2009;284(51):35621–31.
pubmed: 19837661
pmcid: 2790993
doi: 10.1074/jbc.M109.009712
Lopes Barreto D, Krediet RT. Current status and practical use of effluent biomarkers in peritoneal dialysis patients. Am J Kidney Dis. 2013;62(4):823–33.
pubmed: 23669001
doi: 10.1053/j.ajkd.2013.01.031
Stachowska-Pietka J, Poleszczuk J, Flessner MF, Lindholm B, Waniewski J. Alterations of peritoneal transport characteristics in dialysis patients with ultrafiltration failure: tissue and capillary components. Nephrol Dial Transpl. 2019;34(5):864–70.
doi: 10.1093/ndt/gfy313
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(2):116–22.
pubmed: 12713076
doi: 10.1177/089686080302300204
Margetts PJ, Gyorffy S, Kolb M, Yu L, Hoff CM, Holmes CJ, et al. Antiangiogenic and antifibrotic gene therapy in a chronic infusion model of peritoneal dialysis in rats. J Am Soc Nephrol. 2002;13(3):721–8.
pubmed: 11856777
doi: 10.1681/ASN.V133721
Cho Y, Johnson DW, Badve SV, Craig JC, Strippoli GF, Wiggins KJ. The impact of neutral-pH peritoneal dialysates with reduced glucose degradation products on clinical outcomes in peritoneal dialysis patients. Kidney Int. 2013;84(5):969–79.
pubmed: 23698236
doi: 10.1038/ki.2013.190
Johnson DW, Brown FG, Clarke M, Boudville N, Elias TJ, Foo MW, et al. The effect of low glucose degradation product, neutral pH versus standard peritoneal dialysis solutions on peritoneal membrane function: the balANZ trial. Nephrol Dial Transpl. 2012;27(12):4445–53.
doi: 10.1093/ndt/gfs314
Hamada C, Honda K, Kawanishi K, Nakamoto H, Ito Y, Sakurada T, et al. Morphological characteristics in peritoneum in patients with neutral peritoneal dialysis solution. J Artif Organs. 2015;18(3):243–50.
pubmed: 25680950
doi: 10.1007/s10047-015-0822-4
Haas S, Schmitt CP, Arbeiter K, Bonzel KE, Fischbach M, John U, et al. Improved acidosis correction and recovery of mesothelial cell mass with neutral-pH bicarbonate dialysis solution among children undergoing automated peritoneal dialysis. J Am Soc Nephrol. 2003;14(10):2632–8.
pubmed: 14514742
doi: 10.1097/01.ASN.0000086475.83211.DF
Ayuzawa N, Ishibashi Y, Takazawa Y, Kume H, Fujita T. Peritoneal morphology after long-term peritoneal dialysis with biocompatible fluid: recent clinical practice in Japan. Perit Dial Int. 2012;32(2):159–67.
pubmed: 21804136
pmcid: 3525415
doi: 10.3747/pdi.2010.00234
Sieve I, Munster-Kuhnel AK, Hilfiker-Kleiner D. Regulation and function of endothelial glycocalyx layer in vascular diseases. Vascul Pharmacol. 2018;100:26–33.
pubmed: 28919014
doi: 10.1016/j.vph.2017.09.002
Oberleithner H, Peters W, Kusche-Vihrog K, Korte S, Schillers H, Kliche K, et al. Salt overload damages the glycocalyx sodium barrier of vascular endothelium. Pflugers Arch. 2011;462(4):519–28.
pubmed: 21796337
pmcid: 3170475
doi: 10.1007/s00424-011-0999-1
Vlahu CA, Lemkes BA, Struijk DG, Koopman MG, Krediet RT, Vink H. Damage of the endothelial glycocalyx in dialysis patients. J Am Soc Nephrol. 2012;23(11):1900–8.
pubmed: 23085635
pmcid: 3482728
doi: 10.1681/ASN.2011121181
del Peso G, Jimenez-Heffernan JA, Selgas R, Remon C, Ossorio M, Fernandez-Perpen A, et al. Biocompatible dialysis solutions preserve peritoneal mesothelial cell and vessel wall integrity. A case-control study on human biopsies. Perit Dial Int. 2016;36(2):129–34.
pubmed: 26475848
pmcid: 4803356
doi: 10.3747/pdi.2014.00038
Davies SJ. Longitudinal relationship between solute transport and ultrafiltration capacity in peritoneal dialysis patients. Kidney Int. 2004;66(6):2437–45.
pubmed: 15569337
doi: 10.1111/j.1523-1755.2004.66021.x
Lambie M, Chess J, Donovan KL, Kim YL, Do JY, Lee HB, et al. Independent effects of systemic and peritoneal inflammation on peritoneal dialysis survival. J Am Soc Nephrol. 2013;24(12):2071–80.
pubmed: 24009237
pmcid: 3839554
doi: 10.1681/ASN.2013030314
Lambie MR, Chess J, Summers AM, Williams PF, Topley N, Davies SJ, et al. Peritoneal inflammation precedes encapsulating peritoneal sclerosis: results from the GLOBAL Fluid Study. Nephrol Dial Transpl. 2016;31(3):480–6.
doi: 10.1093/ndt/gfv440
Kawanishi H, Kawaguchi Y, Fukui H, Hara S, Imada A, Kubo H, et al. Encapsulating peritoneal sclerosis in Japan: a prospective, controlled, multicenter study. Am J Kidney Dis. 2004;44(4):729–37.
pubmed: 15384025
doi: 10.1016/S0272-6386(04)00953-9
Nakayama M, Kawaguchi Y, Yamada K, Hasegawa T, Takazoe K, Katoh N, et al. Immunohistochemical detection of advanced glycosylation end-products in the peritoneum and its possible pathophysiological role in CAPD. Kidney Int. 1997;51(1):182–6.
pubmed: 8995732
doi: 10.1038/ki.1997.22
Honda K, Nitta K, Horita S, Yumura W, Nihei H, Nagai R, et al. Accumulation of advanced glycation end products in the peritoneal vasculature of continuous ambulatory peritoneal dialysis patients with low ultra-filtration. Nephrol Dial Transpl. 1999;14(6):1541–9.
doi: 10.1093/ndt/14.6.1541