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View of These Earlier Experiences with Sulodexide, It Is Figure 2 CLINICAL RESEARCH www.jasn.org Sulodexide Fails to Demonstrate Renoprotection in Overt Type 2 Diabetic Nephropathy † ‡ ‡ | David K. Packham,* Rory Wolfe, Anne T. Reutens, § Tomas Berl, ‡ †† ‡‡ Hiddo Lambers Heerspink,¶ Richard Rohde,** Sara Ivory, Julia Lewis, Itamar Raz, || Thomas B. Wiegmann,§§ Juliana C.N. Chan, Dick de Zeeuw,¶ Edmund J. Lewis,¶¶ ‡ and Robert C. Atkins, for the Collaborative Study Group *Melbourne Renal Research Group, Melbourne, Australia; †Department of Nephrology, Royal Melbourne and Austin Hospitals, Melbourne, Australia; ‡Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Australia; §Baker IDI Heart and Diabetes Institute, Melbourne, Australia; |Division of Renal Diseases and Hypertension, University of Colorado, Denver, Colorado; ¶Clinical Pharmacology, University Medical Centre Groningen, Groningen, the Netherlands; **The Collaborative Study Group, Chicago, Illinois; ††Division of Nephrology, Vanderbilt University Medical Center, Nashville, Tennessee; ‡‡Diabetes Center, Hadaza Hebrew University, Jerusalem, Israel; §§Renal Service, Veterans Affairs Medical Center, Kansas City, Missouri; ||Department of Medicine and Therapeutics, Chinese University of Hong Kong, Prince of Wales Hospital, Hong Kong, SAR; and ¶¶Rush University Medical Center, Chicago, Illinois ABSTRACT Sulodexide, a mixture of naturally occurring glycosaminoglycan polysaccharide components, has been reported to reduce albuminuria in patients with diabetes, but it is unknown whether it is renoprotective. This study reports the results from the randomized, double-blind, placebo-controlled, sulodexide macroalbuminuria (Sun-MACRO) trial, which evaluated the renoprotective effects of sulodexide in patients with type 2 diabetes, renal impairment, and significant proteinuria (.900 mg/d) already receiving maximal therapy with angiotensin II receptor blockers. The primary end point was a composite of a doubling of base- line serum creatinine, development of ESRD, or serum creatinine $6.0 mg/dl. We planned to enroll 2240 patients over approximately 24 months but terminated the study after enrolling 1248 patients. After 1029 person-years of follow-up, we did not detect any significant differences between sulodexide and placebo; the primary composite end point occurred in 26 and 30 patients in the sulodexide and placebo groups, respec- tively. Side effect profiles were similar for both groups. In conclusion, these data do not suggest a renopro- tective benefit of sulodexide in patients with type 2 diabetes, renal impairment, and macroalbuminuria. J Am Soc Nephrol 23: 123–130, 2012. doi: 10.1681/ASN.2011040378 Diabetic nephropathy is now the most common disease progression in patients with type 2 diabetes cause of ESRD in developed nations.1,2 Type 2 di- with established nephropathy and renal impair- abetic nephropathy accounts for the majority of ment.5,6 This effect is independent of the benefits of patients with diabetes and ESRD.3 The number of BP reduction and seems to correlate with reductions CLINICAL RESEARCH patients with type 2 diabetes mellitus globally is in albuminuria7 and proteinuria.8 Subsequently, expected to double its current levels and reach 366 million persons worldwide by 2030.4 Attempts to alleviate or avert this chronic disease will require Received April 14, 2011. Accepted August 14, 2011. 5 long-term detection and prevention strategies. In Published online ahead of print. Publication date available at the short term, much attention is focused on de- www.jasn.org. veloping proven intervention strategies to alter the Correspondence: Dr. David K. Packham, Melbourne Renal Re- course of diabetic nephropathy. search Group, 73-75 Pine Street, Reservoir, Melbourne, Victoria Studies show that angiotensin receptor blockers 3073, Australia. Email: [email protected] (ARBs) significantly reduce composite end points of Copyright © 2012 by the American Society of Nephrology J Am Soc Nephrol 23: 123–130, 2012 ISSN : 1046-6673/2301-123 123 CLINICAL RESEARCH www.jasn.org ARB use in treatment of type 2 diabetic ne- Table 1. Description of sulodexide and placebo groups in the sulodexide overt phropathy is an established standard of nephropathy trial care; however, ARB use does not abolish Sulodexide Placebo Variable progression to ESRD. Accordingly, re- (n=619)a (n=629)a searchers have investigated, with varying Male, n (%) 383 (79) 376 (74) success, the renoprotective effects of other Age (y), mean (SD) 62.3 (9.4) 63.6 (9.5) agents acting through the renin-angiotensin Height (cm), mean (SD) 168.8 (12.4) 168.5 (11.1) system (RAS)9,10 and of agents with a novel Weight (kg), mean (SD) 93.7 (21.7) 91.1 (21.9) mode of action not involving the RAS.11–13 Body mass index (kg/m2), mean (SD) 33.6 (19.3) 32.3 (12.4) Sulodexide is a mixture of four naturally Total cholesterol (mg/dl), mean (SD) 173.7 (41.5) 179.6 (54.8) occurringglycosaminoglycanpolysaccharide HbA1c (%), mean (SD) 8.0 (1.6) 7.9 (1.5) components isolated from porcine lung Prior CVD, n (%) 227 (47) 233 (46) Family history of CVD, n (%) 304 (63) 335 (66) and liver. Manufacturers have marketed Race, n (%) the drug in many parts of the world for African descent 59 (12) 61 (12) more than 20 years for a range of vascular Asian descent 67 (14) 71 (14) pathologies.14 Preliminary studies show that Caucasian descent 334 (69) 347 (69) sulodexide reduces urinary albumin excre- other 21 (4) 26 (5) tion rates in patients with type 1 and type 2 Use of medication before screening for diabetes.15–22 A number of studies suggest overt trial, n (%) different modes of action to explain this ACE inhibitor only 131 (28) 148 (31%) phenomenon.23–29 ARB only 239 (52) 247 (51%) After conducting a previously reported ACE inhibitor and ARB 62 (13) 62 (13%) pilot study,30 the Collaborative Study none 28 (6) 28 (6%) SeSBP (mmHg), mean (SD) 138.0 (14.0) 138.0 (14.8) Group (CSG) undertook two multina- SeDBP (mmHg), mean (SD) 73.6 (9.9) 73.0 (10.0) tional, randomized, double-blind, placebo- Pulse rate (sitting; beats per min), mean (SD) 69.9 (12.3) 69.3 (11.4) controlled trials using sulodexide in Estimated GFR (ml/min per 1.73 m2), mean (SD) 31.4 (8.7) 31.4 (8.6) patients with type 2 diabetes, and the study Baseline serum creatinine (mg/dl), mean (SD) 2.19 (0.53) 2.16 (0.50) designs were reported in detail previ- PCR,b (mg/g), median (25th–75th percentile) 1836 (990, 3088) 1802 (965, 2966) ously.31 Thesulodexidemicroalbuminuria ACR,b (mg/g), median (25th–75th percentile) 1415 (714, 2400) 1364 (685, 2319) (Sun-MICRO) trial32 was conducted in pa- aData were not available for all participants, and the number with missing data varied for each variable. b tients with preserved renal function and Geometric mean of three values. microalbuminuria. This article reports the results of the sulodexide macroalbuminuria (Sun- During follow-up, 29 participants doubled their baseline MACRO) trial. serum creatinine, 28 reached a serum creatinine of $6.0 mg/dl, and 44 progressed to chronic dialysis. Some participants ex- perienced more than one of these events, and Table 2 shows RESULTS the number of first events for the primary end point (n=56). The sulodexide group had a lower number of primary end We conducted laboratory screening in 2828 patients, with a point events (n=26) than the placebo group (n=30), but this large proportion failing to meet creatinine and/or protein comparison was not statistically significant (hazard ratio: 0.85 inclusion criteria. Inability to satisfy run-in and baseline visit [95% confidence interval: 0.50–1.44]; P=0.54). Thirty-six pa- criteria excluded additional patients. Table 1 presents charac- tients died: 16 in the sulodexide group and 20 in the placebo teristics of the 1248 participants who were randomized (629 to group (P=0.49; Table 3). As shown in Table 3, there was no placebo and 619 to sulodexide) and indicates that the two evidence to attribute any observed imbalances in time to death groups were well balanced at randomization, with no impor- or time to first cardiovascular event to a benefit or harm of tant differences in patient demographics. Figure 1 presents the treatment, nor was there a statistically significant difference in clinical trial randomization flow chart. Figure 2 shows the changes in serum creatinine, proteinuria/creatinine ratio numbers of patients followed up beyond baseline to subse- (PCR), or albumin/creatinine ratio (ACR). Table 4 shows quent visit times. Twenty-seven patients withdrew consent, that serious adverse events were similar in the placebo and and five others were lost to follow-up. Overall, there were sulodexide groups. 1029 person-years of follow-up available. Mean (SD) follow- Aposteriorianalysis identified an early divergence in mean up was 11.2 (6.6) months in the sulodexide group and 10.7 seated systolic BP (SeSBP) between the groups. Three months (6.6) months in the placebo group. Medians were similar to after randomization, mean SeSBP had increased to 139.5 in these means at 11.7 and 9.7 months in the sulodexide and the placebo group but decreased to 137.1 in the sulodexide placebo groups, respectively. group (two-sample t test, P=0.04). 124 Journal of the American Society of Nephrology J Am Soc Nephrol 23: 123–130, 2012 www.jasn.org CLINICAL RESEARCH not regarded as clinically significant. Nodifferences were found in the side effect profiles of sulodexide and placebo and, im- portantly, no serious adverse effects were ascribed to the trial drug. It is important to emphasize that the decision to curtail this trial was not because the Data Safety Monitoring Com- mittee of the CSG had concerns regarding drug toxicity or adverse clinical outcomes. Although the study design required 2240 patients to detect a 20% effect regarding the primary endpoint of doubling initial serum creatinine or ESRD, it is important to note that the secondary outcome of a decrease in proteinuria only required 300–500 patients, a number well below the 1248 patients ran- domized and followed in this trial.
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