Original Article
Effect of Restricting Dietary Protein on the Progression of Renal Failure in Patients with Insulin-Dependent Diabetes Mellitus
N Engl J Med 1991; 324:78-84January 10, 1991
- Abstract
- Abstract
Background.
Restriction of dietary protein may slow the progression of renal failure in diverse renal diseases, but the extent to which such a diet is beneficial in patients with diabetic nephropathy is uncertain.
Methods.
We studied the effect of reduced intake of protein and phosphorus on the progression of renal disease in 35 patients with insulin-dependent (Type I) diabetes mellitus and clinically evident nephropathy. The low-protein, low-phosphorus diet contained 0.6 g of protein per kilogram of ideal body weight per day, 500 to 1000 mg of phosphorus, and 2000 mg of sodium. The control diet consisted of the patient's prestudy diet with the stipulation that it contain 2000 mg of sodium and at least 1 g of protein per kilogram per day and 1000 mg of phosphorus. Renal function was assessed by measurement of iothalamate and creatinine clearances at intervals of 3 to 6 months, and the patients were followed for a minimum of 12 months (mean, 34.7). The declines in mean glomerular filtration rates were compared between groups by linear-regression analysis of the glomerular filtration rate as a function of time.
Results.
The patients who followed the study diet for a mean of 37.1 months had declines in iothalamate clearance of 0.0043 ml per second per month and in creatinine clearance of 0.0055 ml per second per month. The comparable values in the control group were 0.0168 and 0.0135, respectively (P<0.05). Blood pressure was well controlled, and the degree of glycemic control was comparable in both groups.
Conclusions.
Dietary restriction of protein and phosphorus can retard the progression of renal failure in patients with Type I diabetes mellitus who have nephropathy. We believe that wider use of this treatment is indicated. (N Engl J Med 1991; 324:78–84.)
Media in This Article
Figure 1
Progression of Renal Failure in 20 Patients with Diabetic Nephropathy Who Were Following a Low-Protein, Low Phosphorus Diet (Panel A) and in 15 Patients Following a Diet with Normal Intake of Protein and Phosphorus (Panel B·).Table 1
Mean (±SE) Base-Line Characteristics of 35 Patients with Diabetic Nephropathy Who Followed Either the Study Diet or the Control Diet.*Article Activity
- Article
END-STAGE renal disease is one of the most common complications of diabetes mellitus, particularly in patients with insulin-dependent (Type I) diabetes. Although blood glucose control and aggressive management of coexisting hypertension can slow the progression of diabetic nephropathy,1 , 2 progressive renal insufficiency develops in almost half of patients with Type I diabetes.3 4 5 6
Substantial evidence has accumulated in recent years from studies in animals to suggest that restriction of dietary protein and phosphorus can retard the progression of chronic renal failure.7 8 9 10 11 12 13 14 15 16 177 18 19 20 Micropuncture studies performed in rats subjected to subtotal nephrectomy or made diabetic with streptozocin have demonstrated elevations in glomerular pressure and filtration that appear to correlate with progressive renal damage. Increasing levels of urinary protein, hypertension, and progressive loss of renal function developed in these rats. On histologie examination, there was evidence of accumulation in the mesangial matrix, with the eventual occlusion of capillary lumens and capsular space, leading to the formation of sclerotic glomeruli. Restriction of dietary protein reduced the elevated glomerular capillary pressure and filtration in both models of renal disease. In concert with this normalization of glomerular hemodynamics, dietary protein restriction also reduced urinary protein to normal levels and prevented progressive glomerular destruction. Indeed, long-term studies in the sub-total-nephrectomy model have shown marked reduction in the rate of progression to renal failure in rats given a low-protein diet.
In the past several years, clinical investigators have reported variably beneficial results of dietary protein and phosphorus restriction in human subjects. The rates of progression of renal failure have been reduced 2- to 10-fold in groups of patients following a low-protein diet.21 22 23 24 25 These results, however, have come primarily from retrospective, uncontrolled trials of patients with a variety of renal diseases. In this paper we describe the results of a randomized, prospective, controlled trial undertaken to compare the effects of a study diet involving restricted dietary protein and phosphorus and a control diet on the progression of renal failure in patients with a single disease entity —Type I (insulin-dependent) diabetes mellitus.
Methods
Selection of Patients
The entry requirements were Type I diabetes mellitus with onset before the age of 30 years, diabetic nephropathy manifested by proteinuria (24-hour total urinary protein excretion more than 500 mg), concurrent diabetic retinopathy, and the absence of other causes of renal failure. Two treated patients had initial 24-hour urinary protein excretion somewhat less than 500 mg, but they met the other criteria and were therefore included. Whether our data were analyzed with or without these patients did not alter the results. All patients had initial glomerular filtration rates between 15 and 85 percent of the predicted normal values, as determined by measurement of l25I-labeled iothalamate clearance. Reasons for exclusion from the study included contraindications to a low-protein diet, such as severe infection, cancer, or pregnancy, a history of brittle diabetes, age under 18 or over 60 years, and any other condition thought by the patient's primary physician to be a contraindication. A minimum of 12 months of follow-up was required for a patient's inclusion in the analysis, and this interval was defined as the time from enrollment to termination of the study or the patient's withdrawal. The protocol was approved by our institutional review committee, and all patients gave their written informed consent for the study.
We enrolled 47 patients in this trial. Of these, 35 were able to comply with the study requirements and were followed for at least 12 months (mean, 34.7 months). Six to 10 months after the start of the study, two patients in the control-diet group and four patients in the study-diet group were dismissed for inability to comply with appointments, medication schedules, or study diets, or for intravenous drug use. Two additional patients, one from each group, moved away from the area less than one year after enrollment. One patient in the study-diet group died suddenly shortly after enrollment, and one patient in the control-diet group was excluded after the development of severe congestive heart failure due to myocardial infarction. Two additional patients in the study-diet group whose mean protein intakes were 0.85 and 0.80 g per kilogram of body weight per day, with stretches of up to six months during which their protein intake exceeded 0.80 g per kilogram per day, were not excluded, but their results were analyzed separately.
The base-line characteristics of the patients in the two groups are summarized in Table 1Table 1
Mean (±SE) Base-Line Characteristics of 35 Patients with Diabetic Nephropathy Who Followed Either the Study Diet or the Control Diet.*. The groups were similar with regard to age, initial iothalamate clearance, and initial 24-hour urinary protein excretion. One patient in the control-diet group and two patients in the study-diet group were taking angiotensin-converting—enzyme inhibitors to control hypertension. The remainder were treated with some combination of a diuretic agent, clonidine, prazosin, calcium-channel antagonist, beta-adrenergic antagonist, and hydralazine. One patient in the study-diet group was able to discontinue all antihypertensive medications several months after starting the diet.Study Diet
The patients were randomly assigned to one of the two diets. The low-protein diet contained 105 to 167 kj (25 to 40 kcal) per kilogram of ideal body weight per day with 0.6 g of protein per kilogram of ideal body weight per day, of which 70 to 80 percent was high in biologic value. Protein losses in urine were replaced by increasing dietary protein on a gram-for-gram basis. This diet also contained 2000 mg of sodium, 500 to 1000 mg of phosphorus, and 1000 mg of calcium (supplemented with calcium carbonate). The control diet consisted of the patient's prestudy diet, with the stipulation that it contain 2000 mg of sodium and at least 1 g of protein per kilogram of ideal body weight per day and 1000 mg of phosphorus. All the patients received a standard multivitamin preparation. Both the study-diet and control-diet foods were prepared and eaten at home by the patients after receiving instructions at the General Clinical Research Center. All the patients received regular counseling by the study dietitian.
Measurements of Patients
At the time of enrollment, all patients gave a complete history, received a physical examination, and underwent studies of renal function, dietary and nutritional status, and glycemic control. Renal function was evaluated by measurements of urinary protein excretion (24-hour collection), serum creatinine, and creatinine and iothalamate clearance. Dietary protein was estimated from measurements of urinary excretion of urea nitrogen.26 Sodium, potassium, calcium, and phosphorus were also measured in 24-hour urine samples. nutritional status was evaluated by anthropometric measurements and weight, in addition to a complete blood count and determinations of serum concentrations of total protein and albumin. Diabetic control and lipid status were assessed by measurement of glycosylated hemoglobin27 and serum concentrations of total high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, and triglycerides.28 Follow-up evaluation and repeated laboratory studies, including 24-hour urine collections for measurement of creatinine clearance, protein, and urea, complete blood counts, and measurements of serum total protein, albumin, and glycosylated hemoglobin were performed each month for three months and at least every three months thereafter. Iothalamate clearances were measured at three- to six-month intervals, and serum levels of cholesterol, triglycerides, and lipoproteins at six-month intervals.
Chemical analyses of serum and urine were performed by standard clinical laboratory techniques. Glycosylated hemoglobin concentrations were determined by high-performance liquid chromatography,27 and serum levels of cholesterol and triglycerides by spectrophotometric analysis.28 Dietary protein intake was calculated by adding the amount of nitrogen lost in forms other than urea (estimated as 31 mg per kilogram of actual body weight per day) to the measured urinary excretion of urea nitrogen, with adjustment for the level of urinary protein.26 Iothalamate clearance was measured by a method described elsewhere.29 After ingestion of a water load of 20 ml per kilogram and 10 drops of a saturated solution of potassium iodide, 0.75 MBq of l25I-labeled iothalamate was injected subcutaneously. Starting 60 minutes after the injection, three urine samples were collected at 30-minute intervals; plasma samples were collected at 30-minute intervals starting 15 minutes after the first urine collection. Urine and plasma were counted for 1 minute in an Abbott Auto Logic gamma counter, and the iothalamate clearance during each 30-minute period was calculated and the three values averaged. When the three clearance values varied widely, suggesting incomplete voiding, the test was repeated with a Foley catheter or double voiding to collect urine; for these patients, all subsequent measurements were made in the same way. The mean coefficient of variation for the three iothalamate-clearance values was 8.4 percent, as calculated from all measurements performed in March and April of each year of the study.
Blood pressure was measured in three positions (lying, sitting, and standing) in the same arm at each visit. The mean arterial pressure [(systolic blood pressure + [2 X diastolic blood pressure])/3] was calculated in each position, and the results were averaged to provide a single value for each visit. Every effort was made to maintain blood pressure at 140/85 mm Hg or lower, and patients were seen weekly if necessary to maintain good control. The use of angiotensin-converting—enzyme inhibitors was specifically avoided whenever possible. Compliance with the prescribed diet was assessed on the basis of dietary history and measurement of urinary excretion of urea nitrogen. The patients on the study diet who had protein intakes persistently over 0.80 g per kilogram per day and those on the control diet who had protein intakes persistently under 1 g per kilogram per day were excluded from the study.
If patients gave consent, they were followed with fluorescein angiography and funduscopic photography by a retina specialist unaware of the treatment assignment. The degree of retinopathy was graded in each eye with use of a modification of the Early Treatment Diabetic Retinopathy Study system.30 The number of micro-aneurysms was counted separately. The initial and 12-month scores were compared for each patient; changes of more than 2 in the retinopathy grade were considered significant.
Statistical Analysis
The results were analyzed with ISP software developed by the staff of the Academic Computing Services and by the statistician at the General Clinical Research Center with use of CLINFO and BMDP. The rate of deterioration in renal function was analyzed by three methods: regression lines for creatinine and iothalamate clearance and the reciprocal of the serum creatinine value over time were determined for each patient, and the mean slopes were then calculated for each diet group. The initial renal-function values in the patients in the study-diet group were designated as the values measured approximately one month after the institution of the diet. The results were also analyzed by calculating the difference between the initial and the most recent (or final) clearance values and dividing by time.
When more than one measurement for a variable such as blood pressure or urinary excretion of urea nitrogen was obtained within a three-month interval, the values were averaged to provide a single three-month value. The resulting values were then used to determine a mean value for the entire period of follow-up. Student's two-tailed t-test was used to compare the results between treatment groups if the variances were similar, and the Mann—Whitney U test was used if they were not. Stepwise multiple regression analysis was performed with use of the results from the total study population, with the dependent variable being change in glomerular filtration rate and the independent variables being protein intake, blood pressure, and glycosylated hemoglobin concentration. P values less than 0.05 were considered to indicate significance. Results are given as means ±SE.
Results
Progression of Renal Failure
Figure 1Figure 1
Progression of Renal Failure in 20 Patients with Diabetic Nephropathy Who Were Following a Low-Protein, Low Phosphorus Diet (Panel A) and in 15 Patients Following a Diet with Normal Intake of Protein and Phosphorus (Panel B·). shows the iothalamate-clearance values for each patient during the study period, with the mean regression lines indicated by dashed lines. The patients in the study-diet group, with a low intake of protein and phosphorus, had a rate of decline in iothalamate clearance approximately one-fourth that of the patients in the control-diet group, whose protein and phosphorus intakes were normal. Table 2Table 2
Two Assessments of the Rate of Decline of Renal Function in Patients with Diabetic Nephropathy Who Followed Either the Study Diet or the Control Diet. shows the mean rate of decline in the glomerular filtration rate for each group, as determined from linear regression analysis of the creatinine and iothalamate clearances and the reciprocal of the serum creatinine concentration. The rates of decline in both iothalamate and creatinine clearance were significantly slower in the patients in the study-diet group than in those in the control-diet group. As estimated from the reciprocal of the serum creatinine level, the rate of deterioration of renal function was slower, but the difference was not statistically significant. When the decline in renal function was analyzed by calculating the difference between the initial and final (or most recent) clearances and dividing by time, the results were the same (Table 2). The two patients whose mean protein intakes averaged 0.86 and 0.80 g per kilogram per day and who were therefore excluded from the general analysis had stable renal function during a mean follow-up period of 44.5 months.The results for the patients with initial glomerular filtration rates above 0.75 ml per second per 1.73 m2 of body-surface area (mean ±SE, 1.102 ± 0.068; n = 18) were analyzed separately. The rates of renal deterioration, as assessed by linear regression analysis of their iothalamate clearances, were 0.00005±0.0017 ml per second per month in the patients in the study-diet group and 0.0112±0.0037 ml per second per month in the patients in the control-diet group (P<0.05). When the difference between the initial and final iothalamate clearances over time was used to calculate the rate of decline, the decline was 0.00013±0.0017 ml per second per month in the study-diet group and 0.0123 ± 0.0043 ml per second per month in the control-diet group (P<0.05). In the patients with initial glomerular filtration rates below 0.75 ml per second per 1.73 m2 (mean, 0.458±0.033; n = 17), the rates of deterioration of iothalamate clearance were 0.0085±0.0022 ml per second per month in the study-diet group and 0.0235±0.0103 ml per second per month in the control-diet group when measured by regression analysis, and 0.0082 ± 0.0018 and 0.0237±0.01, respectively, when estimated by calculating the difference between the initial and final clearance values. These differences, although large, were not statistically significant.
After approximately three months, the mean urinary protein excretion in the study-diet group fell by 760 mg per 24 hours, as compared with an increase of 928 mg in the control-diet group. At the time of the most recent (or final) determination of the glomerular filtration rate, the patients in the study-diet group had a mean 24-hour urinary protein excretion that was 196 mg less than their mean base-line value (Table 1), whereas the patients in the control-diet group had an increase of 1024 mg. In the study-diet group, marked increases in urinary protein occurred only in the patients whose renal function deteriorated.
Dietary Intake
Each patient's protein intake during the study period was calculated from the measured urinary excretion of urea nitrogen, after normalization for ideal body weight and adjustment for the amount of nitrogen lost in forms other than urea (estimated as 31 mg per kilogram of actual body weight per day) and for the level of urinary protein. The results for each group were then averaged. The patients in the control-diet group consumed a mean of 1.08±0.10 g of protein per kilogram per day, as compared with 0.72 ±0.06 g in the study-diet group (P<0.001) when the two patients whose intakes persistently exceeded 0.80 g per kilogram per day were excluded. The extent of compliance with the protein restriction was calculated as the percentage of protein intake in excess of that prescribed for each patient. During a mean follow-up period of 37.1 months, this excess intake was 11.0±2.3 percent.
Each patient's phosphorus intake during the study was estimated from the measurements of urinary phosphate excretion, after normalization for ideal body weight. The 24-hour urinary excretion of phosphate in the control-diet group was 3.9±0.2 mmol per kilogram, as compared with 2.5±0.1 mmol per kilogram in the study-diet group (P<0.001). Sodium and potassium intake were also estimated from the respective values for 24-hour urinary excretion. There was no difference in potassium intake between groups, the mean values being 59.9±3.9 mmol per 24 hours in the control-diet group and 53.8±3.8 mmol per 24 hours in the study-diet group. The mean sodium intake was slightly but not significantly lower in the study-diet group (134.8±7.3 vs. 158.5±9.9 mmol per 24 hours).
Diabetic Control, Blood Pressure, and Follow-up
Although it has not been demonstrated that improved diabetic control affects the progression of clinically evident nephropathy, we tried to keep this factor constant between the groups of patients. The normal value for glycosylated hemoglobin in our laboratory is less than 5.1 percent of total hemoglobin. During the study, the control-diet group had a mean glycosylated hemoglobin concentration of 8.0±0.4 percent, and the study-diet group had a similar value (7.8±0.2 percent). The institution of the study and control diets did not require substantial adjustments in the insulin dose in either group. Previous investigators have reported an association between systemic hypertension and the rate of progression of renal failure in patients with diabetic nephropathy.1 , 2 The mean arterial pressure in the control-diet group during the study was 105.5±0.9 mm Hg, as compared with 102.3± 1.2 mm Hg in the study-diet group. This difference, although small, was significant at the P = 0.05 level. As stated previously, the antihypertensive regimens used in both groups were comparable, and the target blood pressures identical.
An inverse relation has been reported between the number of visits by patients to the physician and the rate of progression of chronic renal failure.31 We saw the patients in the control-diet group 13.0±1.8 times per year and those in the study-diet group 10.6±1.0 times per year (P not significant). A stepwise regression analysis was performed with the results from the total study population, with the dependent variable being change in the glomerular filtration rate and the independent variables being protein intake, blood pressure, and glycosylated hemoglobin concentration. Protein intake was the only variable that met the selection criteria and was included in the model (r = 0.4178, R2 = 0.1746, P = 0.0139).
nutritional Measures
In the study-diet group, the mean increases in dry body weight, midarm circumference, and serum albumin were 0.40±0.77 kg, 0.04±0.30 cm, and 0.80±0.90 g per liter, respectively, after 12 months. This time point for the comparison of measurements was chosen because all patients were followed for at least 12 months. There was no significant change in any measured nutritional index in the patients following the study diet for an extended period, indicating that this degree of protein restriction did not have adverse nutritional consequences.
Cardiovascular disease is the chief cause of death in patients with Type I diabetes who do not die of renal complications. Since the study diet contained additional calories in the form of carbohydrate and fat, we measured its effect on serum lipids. Table 3Table 3
Serum Lipid Values in 20 Patients with Diabetic Nephropathy before and after One Year of Treatment with the Study Diet. shows the mean serum values initially and after 12 months for cholesterol and triglycerides and the mean ratio between low-density lipoprotein and high-density lipoprotein cholesterol for all patients following the study diet. There was no significant change in any of these values.Infections
Serious infections developed during the study in two patients in the study-diet group and one patient in the control-diet group. The first two patients had a foot ulcer that did not heal and a perforated diverticulum, respectively, that required termination of the low-protein diet after 26 and 22 months. The third patient also had a foot ulcer that did not heal and that required surgery. There was thus no evidence that the study diet resulted in an increased risk of infection.
Progression of Retinopathy
Six patients in the control-diet group and 15 in the study-diet group were followed with fluorescein angiography for at least one year. Of a total of 40 eyes examined during a mean follow-up period of 23.5±2.7 months, 9 eyes of patients in the control-diet group and 22 eyes of patients in the study-diet group showed no change; 2 and 5 eyes, respectively, showed improvement. Only 1 eye in each group deteriorated. There was a small decrease in the number of microaneurysms in both groups (P not significant).
Discussion
Reduced protein intake protects against both the hemodynamic changes of hyperfiltration and the progressive sclerosis of functioning glomeruli in rat models of renal disease ranging from hypertension10 to diabetes9,17 and major renal-mass ablation.8 , 11 12 13 14 15 The relevance of these studies in animals to renal disease in humans is unknown. Although a number of trials in humans have suggested a protective role for restricted intake of protein and phosphorus, these results have been challenged on several grounds.32 , 33 Most studies have dealt with heterogeneous populations, comparing patients with different renal diseases despite the fact that their diseases may not progress at the same rate, if at all.33 In addition, the glomerular filtration rate has generally not been measured directly, with many studies using only the reciprocal of the serum creatinine concentration. Unfortunately, changes in the serum creatinine concentration may not accurately reflect changes in glomerular filtration, particularly when dietary protein intake is altered.34 Since a low-protein diet entails an immediate reduction in the creatine pool, from which creatinine is synthesized, the initiation of such a diet results in an immediate reduction in the serum creatinine level, independently of changes in glomerular filtration. Although a new steady state of creatinine excretion should be achieved within four months, this is only true if muscle mass remains constant. Previous studies have not routinely reported the anthropometric data required to substantiate this. In addition, at low levels of serum creatinine, small variations in results can lead to major differences in estimates of the glomerular filtration rate. Measurements of creatinine clearance should prove more accurate, but they can overestimate the glomerular filtration rate in patients with severe renal insufficiency or diminishing muscle mass,35 and variability in collections may result in poor reproducibility of such measurements.36 For these reasons, clearance of 125I-labeled iothalamate, a radioactive marker similar to inulin, has been recommended as a better indicator of changes in the glomerular filtration rate over time.35
In previous studies, compliance has generally been assessed on the basis of dietary history and sometimes the measurement of urinary urea nitrogen. Since changes in dietary protein intake are primarily reflected in the excretion of urea nitrogen and losses of nitrogen in forms other than urea can be estimated by a factor proportional to weight, the measurement of urinary urea nitrogen is an objective way to assess protein intake accurately, provided that the results are normalized for body weight and adjusted for the level of urinary protein. It is also clear that studies of the effects of low protein intake must control carefully for other potential variables, such as blood pressure and sodium intake.
This prospective, randomized, controlled trial was specifically designed to address these issues. Only patients with a single disease entity, Type I diabetes mellitus, were chosen for study. Renal function was measured according to the clearance of 125I-labeled iothalamate, in addition to the serum creatinine concentration and creatinine clearance. nutritional status was documented according to biochemical and anthropometric criteria, and compliance according to the urinary excretion of urea nitrogen after normalization for body weight and adjustment for losses of urinary protein. Blood pressure and control of diabetes were monitored closely, and dietary intake of sodium was also controlled.
Our results indicate that a low-protein diet can influence the course of diabetic nephropathy markedly. The patients whose protein intake was restricted had a fourfold reduction in the rate of progression of renal failure, as compared with the patients following the control diet, and many patients following the study diet have maintained stable renal function for extended periods (up to 40 months). Nutrition has been well maintained, and there has been no increase in infections. Likewise, there has been no deleterious effect on control of diabetes, lipid status, or retinopathy.
Previous studies1 , 2 have demonstrated that the control of hypertension can reduce the rate of progression of renal failure in patients with Type I diabetes who have nephropathy. Although it is highly unlikely that the difference of 3 mm Hg in mean arterial pressure between treatment groups could have accounted for the difference in the rates of progression, it may have been a contributory factor. Mogensen1 and Parving et al.2 have demonstrated similar degrees of slowing of renal deterioration in diabetic patients treated with comparable antihypertensive programs, but with reductions in mean arterial pressure of 12 and 14 mm Hg, respectively. Björck et al.37 found a significant decrement in the rate of progression of renal failure after a smaller reduction in mean arterial pressure (5 mm Hg), but this result was achieved by the addition of angiotensin-converting—enzyme inhibitors. These drugs were not part of our usual treatment program, precluding meaningful comparison between the study of Björck et al. and our own. The stepwise regression analysis also lends credence to our opinion that differences in blood pressure do not account for these results. Glucose control was comparable between the two groups, and thus it can also be eliminated as a potential variable contributing to the difference in rates of progression. More difficult to exclude is the possibility that decreased phosphorus intake contributed to the beneficial effect of the low-protein diet. Although we and others think this unlikely,38 our findings do not eliminate a potential role for phosphorus intake in the progression of diabetic renal disease.
In summary, dietary restriction of protein and phosphorus can slow the progression of chronic renal failure substantially in patients with diabetic nephropathy. Such a diet does not preclude acceptable glycemic control or result in malnutrition. Further studies are needed to determine the optimal level of protein intake and the point at which protein restriction should be introduced.
Supported by grants from the Juvenile Diabetes Foundation and the Texas Kidney Foundation and by a General Clinical Research Center grant (MOl-RR00633) from the National Institutes of Health.
We are indebted to Drs. Thomas Friberg and George Sanborn for performing periodic retinal examinations and grading the progression of retinopathy, to Ms. Beverly Adams for statistical analysis, and to Mr. John Poindexter and Ms. Terrie Gagliano for assistance in the preparation of the manuscript.
Source Information
From the Department of Internal Medicine (K.Z., E.W., L.S., P.R., H.R.J.) and Center for Human Nutrition (K.Z.), University of Texas Southwestern Medical Center at Dallas. Address reprint requests to Dr. Zeller at the Department of Internal Medicine, University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Blvd., Dallas, TX 75235–8889.
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Bruce A Perkins, Linda H Ficociello, Bijan Roshan, James H Warram, Andrzej S Krolewski. (2010) In patients with type 1 diabetes and new-onset microalbuminuria the development of advanced chronic kidney disease may not require progression to proteinuria. Kidney International 77:1, 57-64
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