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Progression of Microalbuminuria to Proteinuria in Type 1 Diabetes Nonlinear Relationship with Hyperglycemia James H

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Progression of Microalbuminuria to Proteinuria in Type 1 Diabetes Nonlinear Relationship with Hyperglycemia James H Progression of Microalbuminuria to Proteinuria in Type 1 Diabetes Nonlinear Relationship With Hyperglycemia James H. Warram, Laura J. Scott, Linda S. Hanna, Michael Wantman, Shmuel E. Cohen, Lori M.B. Laffe l , Louise Ryan, and Andrzej S. Krolewski While small clinical trials have shown that improved glycemic control reduces the risk of progression of microalbuminuria to proteinuria, two recent clinical n patients with type 1 diabetes, the development of trials did not confirm this finding. We sought to recon- kidney complications, known as diabetic nephropa- cile the contradictory evidence by examining the dose- thy, consists of several stages: the onset of microal- response relationship between hyperglycemia and pro- buminuria, its progression to overt proteinuria, and gression of microalbuminuria to proteinuria in individ- I progression of the proteinuria to end-stage renal disease uals with type 1 diabetes and microalbuminuria (n = 312) who were followed for 4 years with repeated (1,2). Several recent studies clearly demonstrated that the assessments of urinary albumin excretion. Since onset of microalbuminuria is determined by the level of 3 3 patients did not participate in follow-up (10.6%), glycemic control and can be retarded by intensive diabetes data for 279 patients were analyzed. Urinary albumin treatment (3,4). The risk rises exponentially with increasing excretion level worsened to proteinuria in 40 (4.1 per hyperglycemia (5). 100 person-years). To examine the dose-response rela- The role of hyperglycemia in the progression of microal- tionship, baseline HbA1 c was divided into four roughly buminuria to the more advanced stages of nephropathy is equal groups using the cut points 8, 9, and 10%. The inci- un c l e a r , however. Several follow-up studies have demon- dence rate varied significantly among the four groups strated association between progression of microalbuminuria (P = 0.008). Among those with HbA <8.0%, the inci- 1 c and the level of glycemic control (6–9). Moreover, a few small dence rate of progression was only 1.3 per 100 person- years, while it was 5.1, 4.2, and 6.7 per 100 person- clinical trials of intensive insulin therapy indicated that inten- years in the three other groups. We used generalized sive therapy reduces the risk of progression of nephropathy additive models to examine the dose-response curve (10). However, the results of two recent clinical trials did using HbA1 c as a continuous variable and found that the not confirm this conclusion (11,12). risk of progression rises steeply between an HbA1 c o f The present study sought to reconcile the contradictory 7.5–8.5% and then remains approximately constant evidence from the earlier studies by examining the dose- across higher levels. In conclusion, the results of this response relationship between exposure to hyperglycemia study suggest that, in patients with microalbuminuria, and progression of microalbuminuria to overt proteinuria in the risk of progression to overt proteinuria can be the largest cohort studied so far. reduced by improved glycemic control only if the HbA1 c is maintained below 8.5%. Moreover, below that value, RESEARCH DESIGN AND METHODS the risk declines as the level of HbA d e c r e a s e s . 1 c Selection of study subjects. Between 1 January 1991 and 31 March 1992, a 50% D i a b e t e s 4 9 :9 4–100, 2000 sample of the patients aged 15–44 years attending the Internal Medicine or Pedi- atrics departments of the Joslin Diabetes Center was screened for microalbu- minuria in a random urine specimen. By 31 March 1992, 1,602 patients with type 1 diabetes had been screened at least once for microalbuminuria. Subsequently, whenever members of the cohort returned to the clinic, their random urine spec- imens were examined for microalbuminuria. Details of the selection criteria and methods were published with the results of the screening study (5,13), and an abbreviated description is included here. The study protocol was approved by the Committee on Human Studies of the Joslin Diabetes Center. Evaluation of urinary albumin excretion with albumin/creatinine ratio. From the Section of Genetics and Epidemiology (J.H.W., L.J.S., L.S.H., The ratio of urinary concentrations of albumin and creatinine (ACR) measured M . W., S.E.C., L.M.B.L., A.S.K.), Research Division, Joslin Diabetes Center; in random urine samples has become a widely accepted tool for assessing urinary the Departments of Epidemiology (J.H.W., L.J.S., L.S.H., M.W., S.E.C., albumin excretion (UAE) (14–20). Therefore, we used the ACR for both the diag- L.M.B.L., A.S.K.) and Biostatistics (L.R.), Harvard School of Public Health; and Dana-Farber Cancer Institute (L.R.), Boston, Massachusetts. nosis and follow-up of UAE in this study. Urinary albumin concentration was mea- Address correspondence and reprint requests to James H. Warram, MD, sured by immunonephelometry (Behring, Somerville, NJ), and urinary creati- ScD, Genetics and Epidemiology, Joslin Diabetes Center, One Joslin Place, nine concentration was measured by colorimetry (modified Jaffe reaction) on an Boston, MA 02215. E-mail: [email protected]. Astra-7 automated system (Beckman Instruments, Brea, CA). A detailed descrip- Received for publication 11 February 1999 and accepted in revised form tion of laboratory methods has been published (5,13). 28 September 1999. Three levels of UAE were distinguished: normal, microalbuminuria, and overt ACR, albumin/creatinine ratio; DCCT, Diabetes Control and Complications proteinuria. Sex-specific criteria for these levels in terms of the ACR were pub- Trial; GAM, generalized additive model; UAE, urinary albumin excretion. lished previously (13). For men, the lower limits of microalbuminuria and overt 94 DIABETES, VOL. 49, JANUARY 2000 J.H. WARRAM AND ASSOCIATES proteinuria are 17 and 250 µg/mg (1.9 and 28 mg/mmol), respectively. For women, line period. All baseline determinations of glycosylated hemoglobin were measured they are 25 and 355 µg/mg (2.8 and 40 mg / m m o l ) . electrophoretically as HbA1 (Corning Medical and Scientific, Corning, NY.). Since De fi nition of microalbuminuria at baseline. Of the 1,602 patients screened, that time, HbA1c , rather than total HbA1, has become the preferred measure of 38 began dialysis during the baseline period or were found to have a kidney glycemic control. Conversion of our archived HbA1 measurements to HbA1c va l - transplant. They were classified as having overt proteinuria on clinical grounds, ues was validated in the following manner. When the laboratory method was while the remaining 1,564 patients were classified on the basis of ACR measure- changed to ion-exchange high performance liquid chromatography (Va r i a n t ; ments. In a clinical setting, it has been customary to define a patient’s level of UAE Bi o -Rad Laboratories, Hercules, CA) in 1995, both methods were run in parallel according to a consensus of the last three measurements. A category of UAE is for 4 months. The correlation coefficient for duplicate determinations on the same assigned if the level is confirmed by at least two out of three consecutive mea- specimens was 0.98, so we converted all HbA1 values in our data files to HbA1c va l - surements. In this study, we sought to improve on the customary definition by ues (HbA1c = [HbA1 – 0.14]/1.23) (5). In this analysis, we expressed the data as the imposing time constraints on the intervals between measurements. Short-term Hb A 1c values to be consistent with current clinical practice. The normal range in episodes of microalbuminuria (lasting a few weeks) occur in some patients. In this laboratory is 4.0–6.0%. order to detect persistent microalbuminuria instead of these transient episodes, The median number of HbA1c measurements during the two-year baseline we required that the measurements of ACR be separated by a longer period; the period was four. Three or more measurements of HbA1c were obtained for 73% median interval was 5 months (minimum 8 weeks). Furthermore, to define the level of the patients; two measurements were available for 15%, only one measurement of UAE, we used a fixed interval of two years, by which time the majority of for 11%, and none was available for 2%. The geometric mean of all values avail- patients (61%) had at least three ACR determinations. This protocol made the able within the two-year baseline interval was used as the index of glycemic elapsed time for obtaining a classification consistent for all patients and the ex p o s u r e . starting date for follow-up less dependent on visit frequency. It also improved our Treatment with antihypertensive agents. Through a review of medical co n fi dence in the baseline classification by incorporating additional information records and interviews with patients with microalbuminuria, we identified those when more than three tests were available. treated with ACE inhibitors or other antihypertensive agents, either during the Beginning with the date of the initial urine specimen screened for microalbu- baseline interval or subsequently during follow-up. minuria, a 2-year baseline period was defined. The median of all ACR measure- Statistical analysis. Group differences for quantitative variables were tested by ments within the 2-year baseline was used to assign each patient to one of the lev- AN O V A and for qualitative variables by 2 analysis (SAS 6.12 for Windows; SAS els of UAE defined above. For 953 patients (61%), the median was based on 3–12 Institute, Cary, NC). To estimate the incidence rates of proteinuria, a person was samples. Classification of 283 (18%) patients was based on two ACR measurements credited with 2 person-years of follow up for each interval in which they did not that agreed, so a third determination was not necessary to establish a consensus.
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