Free levels of selected organic solutes and cardiovascular morbidity and mortality in hemodialysis patients: Results from the retained organic solutes and clinical outcomes (ROSCO) investigators

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Shafi, Tariq ^a,b   Meyer, Timothy W ^c   Hostetter, Thomas H ^d   Melamed, Michal L ^e   Parekh, Rulan S ^f   Hwang, Seungyoung ^a   Banerjee, Tanushree ^g   Coresh, Josef ^a,b,h   Powe, Neil R ^g  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF TORONTO   (Canada)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 CRESOL SULFATE; ALBUMIN; BETA 2 MICROGLOBULIN; CREATININE; CYSTATIN C; GLUCOSE; HEMOGLOBIN; HIPPURIC ACID; INDICAN; ORGANIC COMPOUND; ORGANIC SOLUTE; PHENYLACETYLGLUTAMINE; PHOSPHATE; POTASSIUM; UNCLASSIFIED DRUG; UREA; 4-CRESOL SULFATE; BIOLOGICAL MARKER; CRESOL; GLUTAMINE; HIPPURIC ACID DERIVATIVE; SULFATE;

ADULT; AGE DISTRIBUTION; ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CAUSE OF DEATH; COHORT ANALYSIS; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; END STAGE RENAL DISEASE; FEMALE; GLUCOSE BLOOD LEVEL; HEMODIALYSIS PATIENT; HIGH RISK POPULATION; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MORBIDITY; OUTCOME ASSESSMENT; PROSPECTIVE STUDY; SENSITIVITY ANALYSIS; STUDY DESIGN; URINE VOLUME; ADVERSE EFFECTS; AGED; ANALOGS AND DERIVATIVES; CARDIOVASCULAR DISEASES; CLINICAL TRIAL; COMPLICATION; HEMODIALYSIS; KIDNEY FAILURE, CHRONIC; METABOLISM; MORTALITY; MULTICENTER STUDY; UNITED STATES;

ADULT; AGED; BIOMARKERS; CARDIOVASCULAR DISEASES; CAUSE OF DEATH; CRESOLS; FEMALE; GLUTAMINE; HIPPURATES; HUMANS; INDICAN; KIDNEY FAILURE, CHRONIC; MALE; MIDDLE AGED; MORBIDITY; MORTALITY; PATIENT OUTCOME ASSESSMENT; RENAL DIALYSIS; SULFURIC ACID ESTERS; UNITED STATES;

EID: 84929377063     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126048     Document Type: Article

References (52)

1. U S Renal Data System, USRDS 2013 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, Maryland. 2015; 4: 2. Available: http://www.usrds.org/atlas13.aspx.
2. Foley RN, Parfrey PS, Sarnak MJ. Epidemiology of cardiovascular disease in chronic renal disease. J Am Soc Nephrol. 1998; 9(12 Suppl):S16-23. PMID: 11443763
3. Dobre M, Meyer TW, Hostetter TH. Searching for uremic toxins. Clin J Am Soc Nephrol. 2013; 8(2):322-7. doi: 10.2215/CJN.04260412 PMID: 23024165
4. Duranton F, Cohen G, De Smet R, Rodriguez M, Jankowski J, Vanholder R, et al. Normal and pathologic concentrations of uremic toxins. J Am Soc Nephrol. 2012; 23(7):1258-70. doi: 10.1681/ASN.2011121175 PMID: 22626821
5. Meyer TW, Hostetter TH. Uremia. N Engl J Med. 2007; 357(13):1316-25. PMID: 17898101
6. Meyer TW, Sirich TL, Hostetter TH. Dialysis cannot be dosed. Semin Dial. 2011; 24(5):471-9. doi: 10.1111/j.1525-139X.2011.00979.x PMID: 21929590
7. Rhee EP, Souza A, Farrell L, Pollak MR, Lewis GD, Steele DJ, et al. Metabolite profiling identifies markers of uremia. J Am Soc Nephrol. 2010; 21(6):1041-51. doi: 10.1681/ASN.2009111132 PMID: 20378825
8. Sirich TL, Funk BA, Plummer NS, Hostetter TH, Meyer TW. Prominent accumulation in hemodialysis patients of solutes normally cleared by tubular secretion. J Am Soc Nephrol. 2014; 25(3):615-22. doi: 10.1681/ASN.2013060597 PMID: 24231664
9. Depner TA. Is Kt/V Urea a Satisfactory Measure for Dosing the Newer Dialysis Regimens? Semin Dial. 2001; 14(1):9-12. PMID: 11208030
10. Meijers BK, Evenepoel P. The gut-kidney axis: indoxyl sulfate, p-cresyl sulfate and CKD progression. Nephrol Dial Transplant. 2011; 26(3):759-61. doi: 10.1093/ndt/gfq818 PMID: 21343587
11. Rechner AR, Smith MA, Kuhnle G, Gibson GR, Debnam ES, Srai SK, et al. Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products. Free Radic Biol Med. 2004; 36(2):212-25. PMID: 14744633
12. Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, et al. Major phenylpropanoidderived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res. 2013; 57(3):523-35. doi: 10.1002/mnfr.201200594 PMID: 23349065
13. Seakins JW. The determination of urinary phenylacetylglutamine as phenylacetic acid. Studies on its origin in normal subjects and children with cystic fibrosis. Clin Chim Acta. 1971; 35(1):121-31. PMID: 5126986
14. Yu L, Blaser M, Andrei PI, Pierik AJ, Selmer T. 4-Hydroxyphenylacetate decarboxylases: properties of a novel subclass of glycyl radical enzyme systems. Biochemistry. 2006; 45(31):9584-92. PMID: 16878993
15. Bammens B, Evenepoel P, Keuleers H, Verbeke K, Vanrenterghem Y. Free serum concentrations of the protein-bound retention solute p-cresol predict mortality in hemodialysis patients. Kidney Int. 2006; 69(6):1081-7. PMID: 16421516
16. Barreto FC, Barreto DV, Liabeuf S, Meert N, Glorieux G, Temmar M, et al. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin J Am Soc Nephrol. 2009; 4(10):1551-8. doi: 10.2215/CJN.03980609 PMID: 19696217
17. Fujii H, Nakai K, Fukagawa M. Role of oxidative stress and indoxyl sulfate in progression of cardiovascular disease in chronic kidney disease. Ther Apher Dial. 2011; 15(2):125-8. doi: 10.1111/j.1744-9987.2010.00883.x PMID: 21426501
18. Liabeuf S, Barreto DV, Barreto FC, Meert N, Glorieux G, Schepers E, et al. Free p-cresylsulphate is a predictor of mortality in patients at different stages of chronic kidney disease. Nephrol Dial Transplant. 2010; 25(4):1183-91. doi: 10.1093/ndt/gfp592 PMID: 19914995
19. Lin CJ, Chuang CK, Jayakumar T, Liu HL, Pan CF, Wang TJ, et al. Serum p-cresyl sulfate predicts cardiovascular disease and mortality in elderly hemodialysis patients. Arch Med Sci. 2013; 9(4):662-8. doi: 10.5114/aoms.2013.36901 PMID: 24049526
20. Lin CJ, Pan CF, Chuang CK, Liu HL, Sun FJ, Wang TJ, et al. Gastrointestinal-related uremic toxins in peritoneal dialysis: a pilot study with a 5-year follow-up. Arch Med Res. 2013; 44(7):535-41. doi: 10.1016/j.arcmed.2013.09.007 PMID: 24055267
21. Lin CJ, Wu CJ, Pan CF, Chen YC, Sun FJ, Chen HH. Serum protein-bound uraemic toxins and clinical outcomes in haemodialysis patients. Nephrol Dial Transplant. 2010; 25(11):3693-700. doi: 10.1093/ndt/gfq251 PMID: 20466687
22. Meijers BK, Claes K, Bammens B, de Loor H, Viaene L, Verbeke K, et al. p-Cresol and cardiovascular risk in mild-to-moderate kidney disease. Clin J Am Soc Nephrol. 2010; 5(7):1182-9. doi: 10.2215/CJN.07971109 PMID: 20430946
23. Meijers BK, Van Kerckhoven S, Verbeke K, Dehaen W, Vanrenterghem Y, Hoylaerts MF, et al. The uremic retention solute p-cresyl sulfate and markers of endothelial damage. Am J Kidney Dis. 2009; 54(5):891-901. doi: 10.1053/j.ajkd.2009.04.022 PMID: 19615803
24. Niwa T. Indoxyl sulfate is a nephro-vascular toxin. J Ren Nutr. 2010; 20(5 Suppl):S2-6. doi: 10.1053/j.jrn.2010.05.002 PMID: 20797565
25. Wu I-W, Hsu K-H, Hsu H-J, Lee C-C, Sun C-Y, Tsai C-J, et al. Serum free p-cresyl sulfate levels predict cardiovascular and all-cause mortality in elderly hemodialysis patients-a prospective cohort study. Nephrol Dial Transplant. 2012; 27(3):1169-75. doi: 10.1093/ndt/gfr453 PMID: 21891772
26. Powe NR, Klag MJ, Sadler JH, Anderson GF, Bass EB, Briggs WA, et al. Choices for Healthy Outcomes in Caring for End Stage Renal Disease. Semin Dial. 1996; 9(1):9-11.
27. Liu Y, Coresh J, Eustace JA, Longenecker JC, Jaar B, Fink NE, et al. Association between cholesterol level and mortality in dialysis patients: role of inflammation and malnutrition. JAMA. 2004; 291(4):451-9. PMID: 14747502
28. Sirich TL, Funk BA, Plummer NS, Hostetter TH, Meyer TW. Prominent accumulation in hemodialysis patients of solutes normally cleared by tubular secretion. J Am Soc Nephrol. 2014; 25(3):615-22. doi: 10.1681/ASN.2013060597 PMID: 24231664
29. Longenecker JC, Klag MJ, Marcovina SM, Liu YM, Jaar BG, Powe NR, et al. High lipoprotein(a) levels and small apolipoprotein(a) size prospectively predict cardiovascular events in dialysis patients. J Am Soc Nephrol. 2005; 16(6):1794-802. PMID: 15800123
30. Miskulin DC, Meyer KB, Athienites NV, Martin AA, Terrin N, Marsh JV, et al. Comorbidity and other factors associated with modality selection in incident dialysis patients: the CHOICE Study. Choices for Healthy Outcomes in Caring for End-Stage Renal Disease. Am J Kidney Dis. 2002; 39(2):324-36. PMID: 11840373
31. Nicolaos VA, Dana CM, Gladys F, Suphamai B, Gertrude S, Marcia L, et al. Comorbidity Assessment in Hemodialysis and Peritoneal Dialysis Using the Index of Coexistent Disease. Semin Dial. 2000; 13(5):320-6. PMID: 11014695
32. Melamed ML, Plantinga L, Shafi T, Parekh R, Meyer TW, Hostetter TH, et al. Retained organic solutes, patient characteristics and all-cause and cardiovascular mortality in hemodialysis: results from the retained organic solutes and clinical outcomes (ROSCO) investigators. BMC Nephrol. 2013; 14(1):134.
33. Donders AR, van der Heijden GJ, Stijnen T, Moons KG. Review: a gentle introduction to imputation of missing values. J Clin Epidemiol. 2006; 59(10):1087-91. PMID: 16980149
34. Singer JD, Willett JB. Applied Longitudinal Data Analysis. New York, NY: Oxford University Press; 2003.
35. Gonthier MP, Remesy C, Scalbert A, Cheynier V, Souquet JM, Poutanen K, et al. Microbial metabolism of caffeic acid and its esters chlorogenic and caftaric acids by human faecal microbiota in vitro. Biomed Pharmacother. 2006; 60(9):536-40. PMID: 16978827
36. Mulder TP, Rietveld AG, van Amelsvoort JM. Consumption of both black tea and green tea results in an increase in the excretion of hippuric acid into urine. Am J Clin Nutr. 2005; 81(1 Suppl):256s-60s. PMID: 15640488
37. Pereira-Caro G, Borges G, van der Hooft J, Clifford MN, Del Rio D, Lean ME, et al. Orange juice (poly) phenols are highly bioavailable in humans. Am J Clin Nutr. 2014; 100(5):1378-84. doi: 10.3945/ajcn.114.090282 PMID: 25332336
38. Rechner AR, Kuhnle G, Hu H, Roedig-Penman A, van den Braak MH, Moore KP, et al. The metabolism of dietary polyphenols and the relevance to circulating levels of conjugated metabolites. Free Radic Res. 2002; 36(11):1229-41. PMID: 12592675
39. Aronov PA, Luo FJ, Plummer NS, Quan Z, Holmes S, Hostetter TH, et al. Colonic contribution to uremic solutes. J Am Soc Nephrol. 2011; 22(9):1769-76. doi: 10.1681/ASN.2010121220 PMID: 21784895
40. Owen WF, Lew NL, Liu Y, Lowrie EG, Lazarus JM. The Urea Reduction Ratio and Serum Albumin Concentration as Predictors of Mortality in Patients Undergoing Hemodialysis. N Engl J Med. 1993; 329(14):1001-6. PMID: 8366899
41. Marquez IO, Tambra S, Luo FY, Li Y, Plummer NS, Hostetter TH, et al. Contribution of residual function to removal of protein-bound solutes in hemodialysis. Clin J Am Soc Nephrol. 2011; 6(2):290-6. doi: 10.2215/CJN.06100710 PMID: 21030575
42. Depner TA. Uremic toxicity: urea and beyond. Semin Dial. 2001; 14(4):246-51. PMID: 11489197
43. Eloot S, Schneditz D, Vanholder R. What can the dialysis physician learn from kinetic modelling beyond Kt/V(urea)? Nephrol Dial Transplant. 2012; 27(11):4021-9. doi: 10.1093/ndt/gfs367 PMID: 22923544
44. Eloot S, Van Biesen W, Glorieux G, Neirynck N, Dhondt A, Vanholder R. Does the adequacy parameter Kt/V(urea) reflect uremic toxin concentrations in hemodialysis patients? PLoS One. 2013; 8(11):e76838. doi: 10.1371/journal.pone.0076838 PMID: 24236005
45. Eloot S, Van Biesen W, Vanholder R. A sad but forgotten truth: the story of slow-moving solutes in fast hemodialysis. Semin Dial. 2012; 25(5):505-9. doi: 10.1111/j.1525-139X.2012.01107.x PMID: 22925227
46. Eloot S, Vanholder R, Van Biesen W. Dialysis Duration: The longer the better, but why? [corrected]. Nephrol Dial Transplant. 2012; 27(11):3975-8. doi: 10.1093/ndt/gfs435 PMID: 23144067
47. Evenepoel P, Meijers BK, Bammens BR, Verbeke K. Uremic toxins originating from colonic microbial metabolism. Kidney Int Suppl. 2009(114:) :S12-9. doi: 10.1038/ki.2009.402 PMID: 19946322
48. Patel KP, Luo FJ, Plummer NS, Hostetter TH, Meyer TW. The production of p-cresol sulfate and indoxyl sulfate in vegetarians versus omnivores. Clin J Am Soc Nephrol. 2012; 7(6):982-8. doi: 10.2215/CJN.12491211 PMID: 22490877
49. Sirich TL, Luo FJ, Plummer NS, Hostetter TH, Meyer TW. Selectively increasing the clearance of protein-bound uremic solutes. Nephrol Dial Transplant. 2012; 27(4):1574-9. doi: 10.1093/ndt/gfr691 PMID: 22231033
50. Vanholder R, Eloot S, Neirynck N, Van Biesen W. Home haemodialysis and uraemic toxin removal: does a happy marriage exist? Nat Rev Nephrol. 2012; 8(10):579-88. doi: 10.1038/nrneph.2012.189 PMID: 22926247
51. Schepers E, Glorieux G, Vanholder R. The gut: the forgotten organ in uremia? Blood Purif. 2010; 29(2):130-6. doi: 10.1159/000245639 PMID: 20093818
52. Poesen R, Meijers B, Evenepoel P. The colon: an overlooked site for therapeutics in dialysis patients. Semin Dial. 2013; 26(3):323-32. doi: 10.1111/sdi.12082 PMID: 23458264