Assessing the validity of surrogate outcomes for ESRD: A meta-analysis

Journal of the American Society of Nephrology

Volumn 26, Issue 9, 2015, Pages 2289-2302

  Jun, Min ^a,b   Turin, Tanvir Chowdhury ^a   Woodward, Mark ^b,c   Perkovic, Vlado ^b   Lambers Heerspink, Hiddo J ^d   Manns, Braden J ^a   Tonelli, Marcello ^a   Hemmelgarn, Brenda R ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; BIOLOGICAL MARKER;

ARTICLE; CHRONIC KIDNEY DISEASE; CREATININE BLOOD LEVEL; DIABETES MELLITUS; END STAGE RENAL DISEASE; HUMAN; META ANALYSIS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN URINE LEVEL; PROTEINURIA; RANDOMIZED CONTROLLED TRIAL (TOPIC); SENSITIVITY ANALYSIS; SYSTEMATIC REVIEW; URINARY EXCRETION; VALIDATION STUDY; BLOOD; KIDNEY FAILURE, CHRONIC; TREATMENT OUTCOME; URINE;

BIOMARKERS; CREATININE; HUMANS; KIDNEY FAILURE, CHRONIC; PROTEINURIA; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TREATMENT OUTCOME;

EID: 84940766795     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014040396     Document Type: Article

References (57)

1. Kidney Disease: Improving GlobalOutcomes (KDIGO) CKDWork Group: KDIGO 2012 Clinical Practice Guideline for the Evaluation and Management of Chronic Kidney Disease. Kidney Int Suppl 3: 1-150, 2013
2. Jha V,Garcia-GarciaG, Iseki K, Li Z,Naicker S, Plattner B, Saran R,Wang AY, Yang CW: Chronic kidney disease: Global dimension and perspectives. Lancet 382: 260-272, 2013
3. Strippoli GF, Craig JC, Schena FP: The number, quality, and coverage of randomized controlled trials in nephrology. J Am Soc Nephrol 15: 411-419, 2004
4. Lambers Heerspink HJ, Perkovic V, de Zeeuw D: Is doubling of serum creatinine a valid clinical 'hard' endpoint in clinical nephrology trials? Nephron 119: c195-c199; discussion c9, 2011
5. Levey AS, Cattran D, Friedman A, Miller WG, Sedor J, Tuttle K, Kasiske B, Hostetter T: Proteinuria as a surrogate outcome in CKD: Report of a scientific workshop sponsored by the National Kidney Foundation and the US Food and Drug Administration. Am J Kidney Dis 54: 205-226, 2009
6. Lambers Heerspink HJ, Weldegiorgis M, Inker LA, Gansevoort R, Parving HH, Dwyer JP, Mondal H, Coresh J, Greene T, Levey AS, de Zeeuw D: Estimated GFR decline as a surrogate end point for kidney failure: A post hoc analysis from the Reduction of End Points in Non-Insulin-Dependent Diabetes With the Angiotensin II Antagonist Losartan (RENAAL) study and Irbesartan Diabetic Nephropathy Trial (IDNT). Am J Kidney Dis 63: 244-250, 2014
7. Stevens LA, Greene T, Levey AS: Surrogate end points for clinical trials of kidney disease progression. Clin JAmSoc Nephrol 1: 874-884, 2006
8. Chen KH, Lin JL, Lin-TanDT, HsuHH, Hsu CW, Hsu KH, Yen TH: Effect of chelation therapy on progressive diabetic nephropathy in patients with type 2 diabetes and high-normal body lead burdens. Am J Kidney Dis 60: 530-538, 2012
9. Endo K, Miyashita Y, Sasaki H, Ohira M, Saiki A, Koide N, Otsuka M, Oyama T, Takeyoshi M, Ito Y, Shirai K: Probucol delays progression of diabetic nephropathy. Diabetes Res Clin Pract 71: 156-163, 2006
10. Facchini FS, Saylor KL: A low-iron-available, polyphenol-enriched, carbohydrate-restricted diet to slow progression of diabetic nephropathy. Diabetes 52: 1204-1209, 2003
11. Baigent C, Landray MJ, Reith C, Emberson J, Wheeler DC, Tomson C, Wanner C, Krane V, Cass A, Craig J, Neal B, Jiang L, Hooi LS, Levin A, Agodoa L,GazianoM, Kasiske B, Walker R,Massy ZA, Feldt-Rasmussen B, Krairittichai U, Ophascharoensuk V, Fellström B, Holdaas H, Tesar V, Wiecek A, Grobbee D, de Zeeuw D, Grönhagen-Riska C, Dasgupta T, Lewis D, HerringtonW,MafhamM,MajoniW,Wallendszus K, GrimmR, Pedersen T, Tobert J, Armitage J, Baxter A, Bray C, Chen Y, Chen Z, Hill M, Knott C, Parish S, Simpson D, Sleight P, Young A, Collins R; SHARP Investigators: The effects of lowering LDL cholesterol with simvastatin plus ezetimibe in patients with chronic kidney disease (Study of Heart and Renal Protection): A randomised placebo-controlled trial. Lancet 377: 2181-2192, 2011
12. Bakris GL, Sarafidis PA, Weir MR, Dahlöf B, Pitt B, Jamerson K, Velazquez EJ, Staikos-Byrne L, Kelly RY, Shi V, Chiang YT, Weber MA; ACCOMPLISH Trial investigators: Renal outcomes with different fixeddose combination therapies in patients with hypertension at high risk for cardiovascular events (ACCOMPLISH): A prespecified secondary analysis of a randomised controlled trial. Lancet 375: 1173-1181, 2010
13. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S; RENAAL Study Investigators: Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345: 861-869, 2001
14. ChoukrounG, KamarN,Dussol B, Etienne I, Cassuto-Viguier E, Toupance O, Glowacki F,Moulin B, Lebranchu Y, TouchardG, JaureguyM, PalletN, LeMeur Y, Rostaing L, Martinez F; CAPRIT study Investigators: Correction of postkidney transplant anemia reduces progression of allograft nephropathy. J Am Soc Nephrol 23: 360-368, 2012
15. Davis TM, Ting R, Best JD, Donoghoe MW, Drury PL, Sullivan DR, Jenkins AJ, O'Connell RL, Whiting MJ, Glasziou PP, Simes RJ, Kesniemi YA, Gebski VJ, Scott RS, Keech AC; Fenofibrate Intervention and Event Lowering in Diabetes Study investigators: Effects of fenofibrate on renal function in patients with type 2 diabetes mellitus: The Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) Study. Diabetologia 54: 280-290, 2011
16. Duckworth W, Abraira C, Moritz T, Reda D, Emanuele N, Reaven PD, Zieve FJ, Marks J, Davis SN, Hayward R, Warren SR, Goldman S, McCarren M, Vitek ME, Henderson WG, Huang GD; VADT Investigators: Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 360: 129-139, 2009
17. Fernandez Juarez G, Luño J, Barrio V, de Vinuesa SG, Praga M, Goicoechea M, Cachofeiro V, Nieto J, Fernández Vega F, Tato A, Gutierrez E; PRONEDI Study Group: Effect of dual blockade of the renin-angiotensin system on the progression of type 2 diabetic nephropathy: a randomized trial. Am J Kidney Dis 61: 211-218, 2013
18. Gouva C, Nikolopoulos P, Ioannidis JP, Siamopoulos KC: Treating anemia early in renal failure patients slows the decline of renal function: A randomized controlled trial. Kidney Int 66: 753-760, 2004
19. Imai E, Chan JC, Ito S, Yamasaki T, Kobayashi F, Haneda M, Makino H; ORIENT study investigators: Effects of olmesartan on renal and cardiovascular outcomes in type 2 diabetes with overt nephropathy: A multicentre, randomised, placebo-controlled study. Diabetologia 54: 2978-2986, 2011
20. Ismail-Beigi F, Craven T, Banerji MA, Basile J, Calles J, Cohen RM, Cuddihy R, Cushman WC, Genuth S, Grimm RH Jr, Hamilton BP, Hoogwerf B, Karl D, Katz L, Krikorian A, O'Connor P, Pop-Busui R, Schubart U, Simmons D, Taylor H, Thomas A, Weiss D, Hramiak I; ACCORD trial group: Effect of intensive treatment of hyperglycaemia on microvascular outcomes in type 2 diabetes: An analysis of the ACCORD randomised trial. Lancet 376: 419-430, 2010
21. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD; The Collaborative Study Group: The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. N Engl J Med 329: 1456-1462, 1993
22. Lewis EJ, Hunsicker LG, Clarke WR, Berl T, Pohl MA, Lewis JB, Ritz E, Atkins RC, Rohde R, Raz I; Collaborative Study Group: Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patientswith nephropathy due to type 2 diabetes.NEngl J Med345: 851-860, 2001
23. Mann JF, Schmieder RE, Dyal L, McQueenMJ, Schumacher H, Pogue J, Wang X, Probstfield JL, Avezum A, Cardona-Munoz E, Dagenais GR, Diaz R, Fodor G, Maillon JM, Rydén L, Yu CM, Teo KK, Yusuf S; TRANSCEND (Telmisartan Randomised Assessment Study in ACE Intolerant Subjects with Cardiovascular Disease) Investigators: Effect of telmisartan on renal outcomes:A randomized trial. Ann InternMed 151: 1-10, W1-2, 2009
24. Mann JF, Schmieder RE, McQueen M, Dyal L, Schumacher H, Pogue J, Wang X, Maggioni A, Budaj A, Chaithiraphan S, Dickstein K, Keltai M, Metsrinne K,Oto A, Parkhomenko A, Piegas LS, Svendsen TL, Teo KK, Yusuf S; ONTARGET investigators: Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (theONTARGET study): A multicentre, randomised, double-blind, controlled trial. Lancet 372: 547-553, 2008
25. MarreM, Lievre M,Chatellier G,Mann JF, Passa P,Ménard J; DIABHYCAR Study Investigators: Effects of low dose ramipril on cardiovascular and renal outcomes in patients with type 2 diabetes and raised excretion of urinary albumin: Randomised, double blind, placebo controlled trial (the DIABHYCAR study). BMJ 328: 495, 2004
26. Parving HH, Brenner BM, McMurray JJ, de Zeeuw D, Haffner SM, Solomon SD, Chaturvedi N, Persson F, Desai AS, NicolaidesM, Richard A, Xiang Z, Brunel P, Pfeffer MA; ALTITUDE Investigators: Cardiorenal end points in a trial of aliskiren for type 2 diabetes. N Engl J Med 367: 2204-2213, 2012
27. Perkovic V, Heerspink HL, Chalmers J, Woodward M, Jun M, Li Q, MacMahon S, Cooper ME, Hamet P, Marre M, Mogensen CE, Poulter N, Mancia G, Cass A, Patel A, Zoungas S; ADVANCE Collaborative Group: Intensive glucose control improves kidney outcomes in patients with type 2 diabetes. Kidney Int 83: 517-523, 2013
28. Ruggenenti P, Perna A, Gherardi G, Garini G, Zoccali C, Salvadori M, Scolari F, Schena FP, Remuzzi G: Renoprotective properties of ACEinhibition in non-diabetic nephropathies with non-nephrotic proteinuria. Lancet 354: 359-364, 1999
29. Ruggenenti P, Perna A, Loriga G, Ganeva M, Ene-Iordache B, Turturro M, Lesti M, Perticucci E, Chakarski IN, Leonardis D, Garini G, Sessa A, Basile C, Alpa M, Scanziani R, Sorba G, Zoccali C, Remuzzi G; REIN-2 Study Group: Blood-pressure control for renoprotection in patients with non-diabetic chronic renal disease (REIN-2): Multicentre, randomised controlled trial. Lancet 365: 939-946, 2005
30. UK Prospective Diabetes Study (UKPDS) Group: Intensive bloodglucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352: 837-853, 1998
31. Wright JT Jr, Bakris G, Greene T, Agodoa LY, Appel LJ, Charleston J, Cheek D, Douglas-Baltimore JG, Gassman J, Glassock R, Hebert L, Jamerson K, Lewis J, Phillips RA, Toto RD, Middleton JP, Rostand SG; African American Study of Kidney Disease and Hypertension Study Group: Effect of blood pressure lowering and antihypertensive drug class on progression of hypertensive kidney disease: Results from the AASK trial. JAMA 288: 2421-2431, 2002
32. Yasuda T, Endoh M, SuzukiD, Yoshimura A, Ideura T, Tamura K, Kamata K, Toya Y, Umemura S, Kimura K; KVT Study Group: Effects of valsartan on progression of kidney disease in Japanese hypertensive patients with advanced, predialysis, chronic kidney disease: Kanagawa Valsartan Trial (KVT). Hypertens Res 36: 240-246, 2013
33. Zucchelli P, Zuccal A, Borghi M, Fusaroli M, Sasdelli M, Stallone C, Sanna G, Gaggi R: Long-term comparison between captopril and nifedipine in the progression of renal insufficiency. Kidney Int 42: 452-458, 1992
34. Hannedouche T, Landais P, Goldfarb B, el Esper N, Fournier A, Godin M, Durand D, Chanard J, Mignon F, Suo JM, et al: Randomised controlled trial of enalapril and beta blockers in non-diabetic chronic renal failure. BMJ 309: 833-837, 1994
35. Prentice RL: Surrogate endpoints in clinical trials: Definition and operational criteria. Stat Med 8: 431-440, 1989
36. Abbate M, Benigni A, Bertani T, Remuzzi G: Nephrotoxicity of increased glomerular protein traffic. Nephrol Dial Transplant 14: 304-312, 1999
37. Remuzzi G, Bertani T: Pathophysiology of progressive nephropathies. N Engl JMed 339: 1448-1456, 1998
38. Abbate M, Zoja C, Morigi M, Rottoli D, Angioletti S, Tomasoni S, Zanchi C, Longaretti L, Donadelli R, Remuzzi G: Transforming growth factor-beta1 is up-regulated by podocytes in response to excess intraglomerular passage of proteins: A central pathway in progressive glomerulosclerosis. Am J Pathol 161: 2179-2193, 2002
39. Hemmelgarn BR, Manns BJ, Lloyd A, James MT, Klarenbach S, Quinn RR, Wiebe N, Tonelli M; Alberta Kidney Disease Network: Relation between kidney function, proteinuria, and adverse outcomes. JAMA 303: 423-429, 2010
40. Iseki K, Ikemiya Y, Iseki C, Takishita S: Proteinuria and the risk of developing end-stage renal disease. Kidney Int 63: 1468-1474, 2003
41. Ninomiya T, Perkovic V, de Galan BE, Zoungas S, Pillai A, Jardine M, Patel A, Cass A, Neal B, Poulter N, Mogensen CE, CooperM, Marre M, Williams B, Hamet P,Mancia G,WoodwardM, Macmahon S, Chalmers J; ADVANCE Collaborative Group: Albuminuria and kidney function independently predict cardiovascular and renal outcomes in diabetes. J Am Soc Nephrol 20: 1813-1821, 2009
42. Perkovic V, Verdon C, Ninomiya T, Barzi F, Cass A, Patel A, JardineM, GallagherM, Turnbull F, Chalmers J, Craig J, Huxley R: The relationship between proteinuria and coronary risk: A systematic review and metaanalysis. PLoS Med 5: e207, 2008
43. Lv J, Ehteshami P, Sarnak MJ, Tighiouart H, Jun M, Ninomiya T, Foote C, Rodgers A, Zhang H, Wang H, Strippoli GF, Perkovic V: Effects of intensive blood pressure lowering on the progression of chronic kidney disease: A systematic review and meta-analysis. CMAJ 185: 949-957, 2013
44. Fallahzadeh MK, Dormanesh B, Sagheb MM, Roozbeh J, Vessal G, PakfetratM, Daneshbod Y, Kamali-Sarvestani E, Lankarani KB: Effect of addition of silymarin to renin-angiotensin system inhibitors on proteinuria in type 2 diabetic patients with overt nephropathy: a randomized, double-blind, placebo-controlled trial. Am J Kidney Dis 60: 896-903, 2012
45. Parving HH, Persson F, Lewis JB, Lewis EJ, Hollenberg NK; AVOID Study Investigators: Aliskiren combined with losartan in type 2 diabetes and nephropathy. N Engl J Med 358: 2433-2446, 2008
46. de Zeeuw D, Agarwal R, Amdahl M, Audhya P, Coyne D, Garimella T, Parving HH, Pritchett Y, Remuzzi G, Ritz E, Andress D: Selective vitamin D receptor activation with paricalcitol for reduction of albuminuria in patients with type 2 diabetes (VITAL study): a randomised controlled trial. Lancet 376: 1543-1551, 2010
47. Lea J, Greene T, Hebert L, LipkowitzM,Massry S,Middleton J, Rostand SG, Miller E, Smith W, Bakris GL: The relationship between magnitude of proteinuria reduction and risk of end-stage renal disease: Results of the African American study of kidney disease and hypertension. Arch Intern Med 165: 947-953, 2005
48. Ruggenenti P, Perna A, Remuzzi G; GISEN Group Investigators: Retarding progression of chronic renal disease: The neglected issue of residual proteinuria. Kidney Int 63: 2254-2261, 2003
49. de Zeeuw D, Remuzzi G, Parving HH, Keane WF, Zhang Z, Shahinfar S, Snapinn S, CooperME,Mitch WE, Brenner BM: Proteinuria, a target for renoprotection in patients with type 2 diabetic nephropathy: Lessons from RENAAL. Kidney Int 65: 2309-2320, 2004
50. Atkins RC, Briganti EM, Lewis JB, Hunsicker LG, Braden G, Champion de Crespigny PJ, DeFerrariG, Drury P, Locatelli F, Wiegmann TB, Lewis EJ: Proteinuria reduction and progression to renal failure in patients with type 2 diabetes mellitus and overt nephropathy. Am J Kidney Dis 45: 281-287, 2005
51. Ruggenenti P, Remuzzi G: Proteinuria: Is the ONTARGET renal substudy actually off target? Nat Rev Nephrol 5: 436-437, 2009
52. TakeuchiN, Takenoshita E, Kato F, Terajima T,Ogawa M, Suzuki S, Fujii T, Kobayashi E, Sakurada T, Satoh N, Ueda S: Doubling of serum creatinine: is it appropriate as the endpoint for CKD? Proposal of a new surrogate endpoint based on the reciprocal of serum creatinine. Clin Exp Nephrol 15: 100-107, 2011
53. Greene T, Teng C-C, Ying J: Validity and statistical power of alternative eGFR-based endpoints: A report from an NKF FDA Workshop. Presented at Kidney Week 2013, Atlanta, GA, November 5-10, 2013 p. TH-PO211.
54. Buyse M, Molenberghs G, Burzykowski T, Renard D, Geys H: The validation of surrogate endpoints in meta-analyses of randomized experiments. Biostatistics 1: 49-67, 2000
55. Inker LA, Levey AS, Pandya K, Stoycheff N, Okparavero A, Greene T; Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI): Early change in proteinuria as a surrogate end point for kidney disease progression: An individual patient meta-analysis. AmJ Kidney Dis 64: 74-85, 2014
56. WoodwardM: Epidemiology: Design andData Analysis, 2ndEd.,Boca Raton, FL, Chapman and Hall/CRC Press, 2005
57. Egger M, Davey Smith G, SchneiderM,Minder C: Bias inmeta-analysis detected by a simple, graphical test. BMJ 315: 629-634, 1997