Diabetes Care
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Published online May 7, 2007
Diabetes Care 30:2034-2039, 2007
DOI: 10.2337/dc07-0140
© 2007 by the American Diabetes Association
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
dc07-0140v1
30/8/2034    most recent
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Rigalleau, V.
Right arrow Articles by Gin, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Rigalleau, V.
Right arrow Articles by Gin, H.
Social Bookmarking
Add to CiteULike   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

Pathophysiology/Complications
Original Article

Normoalbuminuric Renal-Insufficient Diabetic Patients

A lower-risk group

Vincent Rigalleau, MD, PHD1, Catherine Lasseur, MD2, Christelle Raffaitin, MD1, Marie-Christine Beauvieux, PD, PHD3, Nicole Barthe, PD4, Philippe Chauveau, MD2, Christian Combe, MD, PHD2 and Henri Gin, MD, PHD1

1 Department of Nutrition-Diabétologie, Hôpital Haut-Lévêque, Pessac, France
2 Department of Nephrologie, Université Victor Segalen-Bordeaux 2, Hôpital Pellegrin, Bordeaux, France
3 Department of Biochimie, Hôpital Haut-Lévêque, Pessac, France
4 Department of Médecine Nucléaire, Hôpital Pellegrin, Bordeaux, France

Address correspondence and reprint requests to Vincent Rigalleau, Nutrition-Diabétologie, Hôpital Haut-Lévêque, Avenue de Magellan, 33600 Pessac, France. E-mail: vincent.rigalleau{at}wanadoo.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 RESEARCH DESIGN AND METHODS--
 RESULTS
 CONCLUSIONS--
 References
 
OBJECTIVE—About 20% of diabetic patients with chronic kidney disease (CKD) detected from the new American Diabetes Association recommendations (albumin excretion rate >30 mg/24 h or estimated glomerular filtration rate [GFR] <60 ml/min per 1.73 m2) may be normoalbuminuric. Do the characteristics and outcome differ for subjects with and without albuminuria?

RESEARCH DESIGN AND METHODS—A total of 89 patients with diabetes and a modification of diet in renal disease (MDRD) estimated GFR (e-GFR) <60 ml/min per 1.73 m2 underwent a 51Cr-EDTA B-isotopic GFR determination and were followed up for 38 ± 11 months.

RESULTS—The mean MDRD e-GFR (41.3 ± 13.1 ml/min per 1.73 m2) did not significantly differ from the i-GFR (45.6 ± 29.7). Of the subjects, 15 (17%) were normoalbuminuric. Their i-GFR did not differ from the albuminuric rate and from their MDRD e-GFR, although their serum creatinine was lower (122 ± 27 vs. 160 ± 71 µmol/l, P < 0.05): 71% would not have been detected by measuring serum creatinine (sCr) alone. They were less affected by diabetic retinopathy, and their HDL cholesterol and hemoglobin were higher (P < 0.05 vs. albuminuric). None of the CKD normoalbuminuric subjects started dialysis (microalbuminuric: 2/36, macroalbuminuric: 10/38) or died (microalbuminuric: 3/36, macroalbuminuric: 7/38) during the follow-up period (log-rank test: P < 0.005 for death or dialysis), and their albumin excretion rate and sCr values were stable after 38 months, whereas the AER increased in the microalbuminuric patients (P < 0.05), and the sCr increased in the macroalbuminuric patients (P < 0.01).

CONCLUSIONS—Although their sCr is usually normal, most of the normoalbuminuric diabetic subjects with CKD according to an MDRD e-GFR below 60 ml/min per 1.73 m2 do really have a GFR below 60 ml/min per 1.73 m2. However, as expected, because of normoalbuminuria and other favorable characteristics, their risk for CKD progression or death is lower.

Abbreviations: AER, albumin excretion rate • CKD, chronic kidney disease • e-GFR, estimated glomerular filtration rate • GFR, glomerular filtration rate • MDRD, modification of diet in renal disease


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
RESEARCH DESIGN AND METHODS--
 RESULTS
 CONCLUSIONS--
 References
 
Twenty-five to forty percent of patients with diabetes have kidney damage (1), and diabetes is the first cause of end-stage renal disease in most countries (2). The early detection of chronic kidney disease (CKD) in diabetic patients is therefore of critical importance. The conventional approach for screening is the determination of the albumin excretion rate (AER). However, a substantial proportion of normoalbuminuric diabetic patients may present with a reduced glomerular filtration rate (GFR): their rates have been reported to be ~20% based on GFR <60 ml/min per 1.73 m2 in type 2 diabetes (3) and in type 1 diabetes based on GFR <90 ml/min per 1.73 m2 with more advanced glomerular lesions (4). In accordance with the National Kidney Foundation guidelines (5), this has led the American Diabetes Association to recommend the screening of CKD in diabetic patients based both on the AER (threshold: 30 mg/24 h) and the Cockcroft and Gault equation or modification of diet in renal disease (MDRD) equation estimated GFR (threshold: 60 ml/min per 1.73 m2) (6).

The MDRD equation is superior to the Cockcroft and Gault equation: it is more accurate (7,8), more robust when glucose control is poor (9), and not biased by body weight (10), which is of considerable importance because of the frequent association of type 2 diabetes, and CKD (11), with obesity. Most of the recent reports on CKD in diabetic patients rely on MDRD e-GFR (12–16). This equation may however not be ideal for screening CKD, as it is known to underestimate normal and high GFR (17,18): some of the MDRD-based CKD diagnosis may stem from this underestimation (19), particularly in normoalbuminuric patients. Furthermore, the progressive nature of normoalbuminuric CKD has been argued from studies based on measured GFR, reported by one group (3,20), and its association with complications relies on reports in Asian diabetic subjects, who are known to have a high incidence of CKD (14). Whether this applies to MDRD-diagnosed normoalbuminuric CKD in Caucasians remains to be demonstrated.

To evaluate the significance of normoalbuminuric CKD in diabetes, we compared the isotopic GFR and serum creatinine of normoalbuminuric versus albuminuric diabetic patients with CKD according to an MDRD e-GFR <60 ml/min per 1.73 m2. The baseline characteristics of the patients, and their outcome during a 38-month follow-up, were also compared.


   RESEARCH DESIGN AND METHODS—
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS--
RESULTS
 CONCLUSIONS--
 References
 
A total of 89 patients (49 men, mean age 64 ± 11 years) were recruited from the Nutrition-Diabetology and Nephrology departments of the Centre Hospitalier Universitaire de Bordeaux. The inclusion criteria were as follows: 1) diabetes (a total of 22 patients had type 1 diabetes and 67 had type 2 diabetes) and 2) CKD according to an MDRD e-GFR <60 ml/min per 1.73 m2, not requiring renal replacement therapy at inclusion.

The patients gave written informed consent to participate in the study, which was approved by the ethical committee of our institution. This study was supported by a clinical research program in the Bordeaux University Hospital.

Analytical methods
The AER was determined on one 24-h urine collection during a short hospitalization, with an immunonephelometric analyzer (Behring Nephelometer 2) using an appropriate kit (Nantiserum VO human albumin; Dade Behring). Serum creatinine was determined on a multiparameter analyzer (Olympus AU 640; Olympus Optical, Tokyo, Japan), using the Jaffé method with bichromatic measurements according to the manufacturer's specifications, and daily calibration of the analyzer. This procedure did not change in our laboratory during the study. Clearance of the radionuclide marker was measured after intravenous injection of 51Cr-EDTA (Cis Industries, Gif/Yvette, France). All patients were studied in the morning at 9:00 A.M., after a light breakfast. After a single bolus of 100 µCi (3.7 MBq) of 51Cr-EDTA, four venous blood samples were drawn at 75, 105, 135, and 165 min, and urinary samples were collected at 90, 120, 150, and 180 min, as previously described (21). The final result was the mean of the four clearance values. If for one period, the urine flow was too low or if a clearance value was not within ±20% of the mean of the three others, this value was excluded and the mean was calculated for the other three clearances. Less than 5% of the values were excluded this way. The 51Cr-EDTA radioactivity was measured in a gamma counter (COBRA 2, model 05003; Packard Instruments, Meriden, CT).

Follow-up, care, and outcome
This prospective study began in June 2001. It was based on a cooperative follow-up between diabetologists and nephrologists with the establishment of a joint medical file for each patient. This cooperative follow-up was complementary and included one visit with the diabetologist every 4 months and one visit with the nephrologist every year if 40 < MDRD e-GFR ≤60 ml/min per 1.73 m2, every 4 months if 20 < MDRD e-GFR ≤40 ml/min per 1.73 m2, and then one visit every 1 or 2 months if MDRD e-GFR ≤20 ml/min per 1.73 m2. Mean duration of the follow-up was 38 ± 11 months.

The care program objectives included glycemic control according to the French 1999 recommendations (A1C <8.0%; if possible, 6.5% without severe hypoglycemia in type 2 and <7.0% in type 1 diabetes), but also control of associated factors such as hypertension (objective: <130/80 mmHg) and dyslipidemia (objective: LDL cholesterol <1.3 g/l). We prescribed 0.8 g protein · kg–1 · day–1 according to the National Kidney Foundation recommendations (22), except for patients with clinical signs of undernutrition or who were ≥65 years of age.

The primary outcome was requirement for dialysis, or death. The secondary outcomes were the AER and serum creatinine for living nondialyzed patients at the end of the follow-up.

Statistical analysis
The results are expressed as means ± SD. The normoalbuminuric patients were compared with the albuminuric (micro- and macroalbuminuric) patients by ANOVA and unpaired Student's t tests for the continuous variables and by {chi}2 test for the categorical variables. Similar analysis was performed after categorizing the subjects as normoalbuminuric (AER <30 mg/24 h), microalbuminuric (30 ≤ AER <300 mg/24 h), and macroalbuminuric (AER ≥300 mg/24 h), with a Bonferroni correction. For the primary outcome (death or dialysis), prognostic curves were obtained using the Kaplan-Meier estimation method and compared by log-rank test; the patients who did not present any event (death or dialysis onset) were censored at the end of the follow-up. For the secondary outcome, the baseline and final characteristics of the patients were compared by paired Student's t tests. All the analysis was performed using SPSS software, version 10.0. The significance level was fixed at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS--
 RESULTS
CONCLUSIONS--
 References
 
Baseline characteristics
A total of 89 patients were included. Their mean diabetes duration was 18 ± 10 years, mean MDRD e-GFR was 41.3 ± 13.1 ml/min per 1.73 m2 (11–59.9), it did not significantly differ from their isotopic GFR (45.6 ± 29.7, P = 0.12), although 15 subjects had an isotopic GFR >60 ml/min per 1.73 m2. A total of 15 subjects (17%) were normoalbuminuric. The proportion of subjects whose isotopic GFR was >60 ml/min per 1.73 m2 was lower in the normoalbuminuric group (13.3%) than the normoalbuminuric group (25.7%, NS by {chi}2). The normoalbuminuric subjects were less frequently affected by diabetic retinopathy, but they had higher HDL cholesterol and hemoglobin levels. For these characteristics, the difference was mainly due to the macroalbuminuric group, with intermediary values in the microalbuminuric group. There were also tendencies (P < 0.07) for more women, less cigarette smoking, fewer previous cardiac events, a lower duration of diabetes, and a higher total cholesterol level in the normoalbuminuric group. The type of diabetes, A1C, and blood pressure did not differ (Table 1).


View this table:
[in this window]
[in a new window]

  		Table 1— Baseline characteristics of patients

 
Most of the normoalbuminuric patients (71%) had serum creatinine levels in the normal range. Despite their lower serum creatinine levels, their MDRD e-GFR did not significantly differ from the albuminuric group, and the MDRD underestimation was not significant in either group (P = 0.051 between isotopic and MDRD e-GFR in the microalbuminuric group). The correlation between MDRD e-GFR and the reference isotopic measurement was even better for the normoalbuminuric group, and the accuracy of the MDRD (percent estimations within ±10, 30, and 50% of the isotopic GFR) tended to be better for them. The coexistence of normal AER and CKD could therefore not be attributed to the MDRD underestimation of GFR in our patients.

Outcome
Primary outcome.
Ten of the albuminuric patients died during the follow-up, whereas all the normoalbuminuric subjects were alive at its end. Twelve of the albuminuric patients required dialysis during the follow-up (10 from the macroalbuminuric patients, P < 0.01 by {chi}2), whereas none of the normoalbuminuric patients did. Figure 1 shows the log survival curve, with dialysis or death as the end point.


Figure 1
View larger version (16K):
[in this window]
[in a new window]

  		Figure 1— Log survival plot (end point: death or dialysis).

 
Secondary outcome.
The second AER and serum creatinine determination was performed in all the alive nondialized patients. The changes in AER, serum creatinine, and MDRD e-GFR did not significantly differ according to baseline normo-, micro-, and macroalbuminuria. However, normoalbuminuria persisted during the follow-up, and serum creatinine did not change in the normoalbuminuric group. By contrast, AER increased in the microalbuminuric patients (P < 0.05 vs. baseline), and serum creatinine increased in the macroalbuminuric patients (P < 0.01 vs. baseline). The MDRD e-GFR tended to decrease in the albuminuric patients (P = 0.05), and the comparison between baseline and final values only involved the subjects who did not have to start hemodialysis (12 albuminuric patients, none normoalbuminuric) (Table 2).


View this table:
[in this window]
[in a new window]

  		Table 2— Outcome characteristics of patients at the end of follow-up

 

   CONCLUSIONS—
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS--
 RESULTS
 CONCLUSIONS--
References
 
Our first objective was to find out whether normoalbuminuric diabetic patients might represent an artificial group, stemming from overdiagnosed CKD due to the underestimation of high GFR by the MDRD equation. The isotopic determination of GFR in our patients argues against this hypothesis: although the MDRD underestimated their GFR, the difference was slight and not significant. The proportion of subjects for which isotopic GFR was >60 ml/min per 1.73 m2 was indeed lower in the normoalbuminuric group (13.3%) than in the normoalbuminuric group (25.7%, NS by {chi}2), and the correlation between estimated and measured GFR was better in the normoalbuminuric group. Most of these patients, therefore, really had a GFR <60 ml/min per 1.73 m2, which would have been missed for 71% of them if their renal function had been assessed solely by a serum creatinine level >120 µmol/l. Despite its underestimation of GFR, mainly for GFR >60 ml/min per 1.73 m2 (18,23), and the increase in the number of detected CKD (12,24), the use of the MDRD equation as recommended by the American Diabetes Association is of interest, especially when AER is normal.

Apart from their relatively low creatinine levels, our normoalbuminuric CKD patients displayed a number of specific characteristics: a higher proportion of women, a lower duration of diabetes, a low prevalence of retinopathy (3,4), fewer smokers (25), higher hemoglobin levels (26,27), and higher HDL cholesterol (28,29) are consistent with previous reports on the characteristics associated with the presence of an abnormal AER. As our normoalbuminuric patients were mainly women and slightly older, their low MDRD e-GFR was not unexpected: increasing age and female sex both reduce the MDRD estimation. Only a minority of these patients had diabetic retinopathy, suggesting that their renal impairment may not be due to diabetic nephropathy. However, around one-third of type 2 diabetic patients with renal biopsy–demonstrated diabetic glomerulopathy do not have retinopathy (30). Because blood pressure levels did not differ between the two groups, it seems unlikely that the low GFR of normoalbuminuric patients was due to nephroangiosclerosis; these patients were also less affected by previous cardiovascular events. However, they required as much antihypertensive therapy as did the albuminuric patients, which suggests that their renal impairment was not without consequence.

Although 17 is similar to the 20 normoalbuminuric patients studied by MacIsaac et al. (3), the small sample size is a limitation of our study, which probably explains why the differences between AER and e-GFR changes did not reach significance. Formulae estimations are known to underestimate the decline in GFR in diabetic patients (31). None of the normoalbuminuric patients died or started dialysis, and their stable AER and serum creatinine, whereas AER increased in microalbuminuric, and creatinine increased in the macroalbuminuric, both significantly, are however strong indications for a better outcome in the normoalbuminuric group. It must be noticed that most of the clinical events occurred in CKD patients with macroalbuminuria. The different characteristics we found may have contributed to this better outcome: male sex (32), a longer duration of diabetes (33), the presence of retinopathy (34), a lower hemoglobin level (32,35), and smoking (36) have all been reported to be associated with the progression of nephropathy in diabetes. However, the most probable is the persisting absence of albuminuria by itself: numerous reports have emphasized its importance for CKD progression (30,33–35,37,38) and coronary heart disease (39) in diabetes.

Some other limitations should be noted. As reflected by the scatter of the isotopic GFR in the albuminuric group (Table 1), their proportion of stages 4–5 CKD was higher (26/74 vs. 3/15 normoalbuminuric), which can explain that all the subjects who had to start dialysis were albuminuric. We feel nonetheless that the few severe and terminal CKD cases in the normoalbuminuric group is a reflection that it is, on the whole, a rather stable condition. Silveiro et al. (40) studied the evolution over 5 years of 51Cr-EDTA–determined GFR in 32 normoalbuminuric type 2 diabetic subjects: their GFR decline (–0.18 ml/min per month) did not differ from normal subjects (–0.14), except for 13 subjects who were hyperfiltering at baseline (–0.61). Nine of our normoalbuminuric patients were treated by ACE inhibitors or angiotensin receptor blockers. Although their proportion did not differ from the albuminuric group, these treatments may have contributed to their good outcome, but we cannot be sure of this because we do not know whether they had abnormal AER before the initiation of these medications. Finally, because no renal biopsy was performed in our patients, their renal impairment may not have been due to diabetic nephropathy, which would account for their better outcome (30). However, we feel that whether our patients actually had diabetic nephropathy is not the issue: our purpose was to determine the outcomes in patients with diabetes and a reduced estimated GFR, classified as presenting CKD according to the new recommendations. Of such patients, 17% were normoalbuminuric in our study. Our isotopic determination of GFR confirmed that they really had GFR below 60 ml/min per 1.73 m2, although most of them would have not been detected on the sole basis of their serum creatinine level. But they did not progress, and the necessity to measure estimated GFR by MDRD, and label these patients as having CKD, may result in adverse emotional and financial consequences. Further studies on the outcome of normoalbuminuric CKD in diabetes are required to demonstrate that the awareness of this condition is a benefit.


   Acknowledgments
 
This study was supported by a grant from the Programme Hospitalier de Recherche Clinique 2001.

We would like to thank Dr. Simon Jarman for revision of the English manuscript.


   Footnotes
 
Published ahead of print at http://care.diabetesjournals.org on 7 May 2007. DOI: 10.2337/dc07-0140.

A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C Section 1734 solely to indicate this fact.

Received for publication January 23, 2007. Accepted for publication April 29, 2007.


   References
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS--
 RESULTS
 CONCLUSIONS--
 References
 

  1. Parving HH: Renoprotection in diabetes: genetic and non-genetic risk factors and treatment. Diabetologia 41:745–759, 1998[Medline]
  2. 1999 United States Renal Data System Annual Report. National Technical Information Service, U.S. Department of Health and Human Services, Springfield, VA, 1999
  3. MacIsaac RJ, Tsalamandris C, Panagiotopoulos S, Smith TJ, McNeil KJ, Jerums G: Nonalbuminuric renal insufficiency in type 2 diabetes. Diabetes Care 27:195–200, 2004[Abstract/Free Full Text]
  4. Caramori ML, Fioretto P, Mauer M: Low glomerular filtration rate in normoalbuminuric type 1 diabetic patients: an indicator of more advanced glomerular lesions. Diabetes 52:1036–1040, 2003[Abstract/Free Full Text]
  5. Levey AS, Coresh J, Balk E, Kausz AT, Levin A, Steffes MW, Hogg RJ, Perrone RD, Lau J, Eknoyan G: National Kidney Foundation Practice Guidelines for chronic kidney disease: evaluation, classification and stratification. Ann Intern Med 139:137–147, 2003[Abstract/Free Full Text]
  6. Kramer H, Molitch ME: Screening for kidney disease in adults with diabetes. Diabetes Care 28:1813–1816, 2005[Free Full Text]
  7. Rigalleau V, Lasseur C, Perlemoine C, Barthe N, Raffaitin C, Liu C, Chauveau P, Baillet-Blanco L, Beauvieux MC, Combe C, Gin H: Estimation of glomerular filtration rate in diabetic patients: Cockcroft or MDRD formula? Diabetes Care 28:838–843, 2005[Abstract/Free Full Text]
  8. Poggio ED, Wang X, Greene T, Van Lente F, Hall PM: Performance of the modification of diet in renal disease and Cockcroft-Gault equations in the estimation of GFR in health and in chronic kidney disease. J Am Soc Nephrol 16:459–466, 2005[Abstract/Free Full Text]
  9. Rigalleau V, Lasseur C, Raffaitin C, Perlemoine C, Barthe N, Chauveau P, Combe C, Gin H: Glucose control influences glomerular filtration rate and its prediction in diabetic subjects. Diabetes Care 29:1491–1495, 2006[Abstract/Free Full Text]
  10. Rigalleau V, Lasseur C, Perlemoine C, Barthe N, Raffaitin C, Chauveau P, Combe C, Gin H: Cockcroft-Gault formula is biased by body weight in diabetic patients with renal impairment. Metabolism 55:108–112, 2006[Medline]
  11. Ejerblad E, Fored M, Linblad P, Fryzek J, McLaughlin JK, Nyrén O: Obesity and risk for chronic renal failure. J Am Soc Nephrol 17:1695–1702, 2006[Abstract/Free Full Text]
  12. Middleton RJ, Foley RN, Hegarty J, Cheung CM, McElduff P, Gibson JM, Kalra PA, O'Donoghue DJ, New JP: The unrecognized prevalence of chronic kidney disease in diabetes. Nephrol Dial Transplant 21:88–92, 2006[Abstract/Free Full Text]
  13. Thomas MC, Tsalamandris C, MacIsaac RJ, Jerums G: The epidemiology of hemoglobin levels in patients with type 2 diabetes. Am J Kidney Dis 48:537–545, 2006[Medline]
  14. Kong AP, So WY, Szeto CC, Chan NN, Luk A, Ma RC, Ozaki R, Ng VW, Ho CS, Lam CW, Chow CC, Cockram CS, Chan JC, Tong PC: Assessment of glomerular filtration rate in addition to albuminuria is important in managing type II diabetes. Kidney Int 69:383–387, 2006[Medline]
  15. So WY, Kong APS, Ma RCW, Ozaki R, Szeto CC, Chan NN, Ng V, Ho CS, Lam CW, Chow CC, Cockram CS, Chan JC, Tong PC: Glomerular filtration rate, cardiorenal end points, and all-cause mortality in type 2 diabetic patients. Diabetes Care 29:2046–2052, 2006[Abstract/Free Full Text]
  16. De Cosmo S, Lamacchia O, Rauseo A, Viti R, Gesualdo L, Pilotti L, Trischitta V, Cignarelli M: Cigarette smoking is associated with low glomerular filtration rate in male patients with type 2 diabetes. Diabetes Care 29:2467–2470, 2006[Abstract/Free Full Text]
  17. Froissard M, Rossert J, Jacquot C, Paillard M, Houiller P: Predictive performance of the modification of diet in renal disease and Cockcroft-Gault equations for estimating renal function. J Am Soc Nephrol 16:763–773, 2005[Abstract/Free Full Text]
  18. Rigalleau V, Lasseur C, Raffaitin C, Perlemoine C, Barthe N, Chauveau P, Combe C, Gin H: The Mayo Clinic quadratric equation improves the prediction of the glomerular filtration rate in diabetic subjects. Nephrol Dial Transplant 22:813–818, 2007[Abstract/Free Full Text]
  19. Rigalleau V, Lasseur C, Chauveau P, Raffaitin C, Perlemoine C, Barthe N, Combe C, Gin H: Is the diagnosis of chronic kidney disease missed in diabetic women? Nephrol Dial Transplant 21:1732–1733, 2006[Free Full Text]
  20. Tsalamandris C, Allen TJ, Gilbert RE, Sinha A, Panagiotopoulos S, Cooper ME, Jerums G: Progressive decline in renal function in diabetic patients with and without albuminuria. Diabetes 43:649–655, 1994[Abstract]
  21. Combe C, Deforges-Lasseur C, Caix J, Pommereau A, Marot D, Aparicio M: Compliance and effects of nutritional treatment on progression and metabolic disorders of chronic renal failure. Nephrol Dial Transplant 8:412–418, 1993[Abstract/Free Full Text]
  22. National Kidney Foundation: Kidney disease outcome quality initiative: clinical practice guidelines for nutrition in chronic renal failure. I. Adult guidelines. B. Advanced chronic renal failure without dialysis. Am J Kidney Dis 35:S56–S65, 2000
  23. Ibrahim H, Mondress M, Tello A, Fan Y, Koopmeiners J, Thomas W: An alternative formula to the Cockcroft-Gault and the modification of diet in renal diseases formulas in predicting GFR in individuals with type 1 diabetes. J Am Soc Nephrol 16:1051–1060, 2005[Abstract/Free Full Text]
  24. Kramer HJ, Nguyen QD, Curhan G, Hsu CY: Renal insufficiency in the absence of albuminuria and retinopathy among adults with type 2 diabetes mellitus. JAMA 289:3273–3277, 2003[Abstract/Free Full Text]
  25. Scott LJ, Warram JH, Hanna LS, Laffel LM, Ryan L, Krolewski AS: A nonlinear effect of hyperglycemia and current cigarette smoking are major determinants of the onset of microalbuminuria in type 1 diabetes. Diabetes 50:2842–2849, 2001[Abstract/Free Full Text]
  26. Thomas MC, MacIsaac RJ, Tsalamandris C, Molyneaux L, Goubina I, Fulcher G, Yue D, Jerums G: Anemia in patients with type 1 diabetes. J Clin Endocrinol Metab 89:4359–4363, 2004[Abstract/Free Full Text]
  27. Thomas MC, MacIsaac RJ, Tsalamandris C, Molyneaux L, Goubina I, Fulcher G, Yue D, Jerums G: The burden of anaemia in type 2 diabetes and the role of nephropathy: a cross-sectional audit. Nephrol Dial Transplant 19:1792–1797, 2004[Abstract/Free Full Text]
  28. Jones SL, Close CF, Mattock MB, Jarrett RJ, Keen H, Viberti GC: Plasma lipid and coagulation factor concentrations in insulin dependent diabetics with microalbuminuria. BMJ 298:487–490, 1989[Medline]
  29. Niskanen L, Uusitupa M, Sarlund H, Siitonen O, Voutilainen E, Penttila I, Pyorala K: Microalbuminuria predicts the development of serum lipoprotein abnormalities favouring atherogenesis in newly diagnosed type 2 (non-insulin-dependent) diabetic patients. Diabetologia 33:237–243, 1990[Medline]
  30. Christensen PK, Gall MA, Parving HH: Course of glomerular filtration rate in albuminuric type 2 diabetic patients with or without diabetic glomerulopathy. Diabetes Care 23 (Suppl. 2):B14–B20, 2000
  31. Rossing P, Rossing K, Gaede P, Pedersen O, Parving HH: Monitoring kidney function in type 2 diabetic patients with incipient and overt diabetic nephropathy. Diabetes Care 29:1024–1030, 2006[Abstract/Free Full Text]
  32. Ueda H, Ishimura E, Shoji T, Emoto M, Morioka T, Matsumoto N, Fukumoto S, Miki T, Inaba M, Nishizawa Y: Factors affecting progression of renal failure in patients with type 2 diabetes. Diabetes Care 26:1530–1534, 2003[Abstract/Free Full Text]
  33. Bruno G, Biggeri A, Merletti F, Bargero G, Ferrero S, Pagano G, Perin PC: Low incidence of end-stage renal disease and chronic renal failure in type 2 diabetes: a 10-year prospective study. Diabetes Care 26:2353–2358, 2003[Abstract/Free Full Text]
  34. Trevisan R, Vedovato M, Mazzon C, Coracina A, Iori E, Tiengo A, Del Prato S: Concomitance of diabetic retinopathy and proteinuria accelerates the rate of decline of kidney function in type 2 diabetic patients. Diabetes Care 25:2026–2031, 2002[Abstract/Free Full Text]
  35. Babazono T, Hanai K, Suzuki K, Kiuchi Y, Inoue A, Tanaka M, Tanaka N, Hase M, Ishii A, Iwamoto Y: Lower haemoglobin level and subsequent decline in kidney function in type 2 diabetic adults without clinical albuminuria. Diabetologia 49:1387–1393,2006
  36. Stegmayr B, Lithner F: Tobacco and end stage diabetic nephropathy. BMJ 295:581–582, 1987[Medline]
  37. Jacobsen P, Rossing K, Tarnow L, Rossing P, Mallet C, Poirier O, Cambien F, Parving HH: Progression of diabetic nephropathy in normotensive type 1 diabetic patients. Kidney Int Suppl 71:S101–S105, 1999[Medline]
  38. Rossing K, Christensen PK, Hovind P, Tarnow L, Rossing P, Parving HH: Progression of nephropathy in type 2 diabetic patients. Kidney Int 66:1596–1605, 2004[Medline]
  39. Mattock MB, Barnes DJ, Viberti G, Keen H, Burt D, Hughes JM, Fitzgerald AP, Sandhu B, Jackson PG: Microalbuminuria and coronary heart disease in NIDDM: an incidence study. Diabetes 47:1786–1792, 1998[Abstract]
  40. Silveiro SP, Friedman R, de Azevedo MJ, Canani LH, Gross JL: Five-year prospective study of glomerular filtration rate and albumin excretion rate in normofiltering and hyperfiltering normoalbuminuric NIDDM patients. Diabetes Care 19:171–174, 1996[Abstract]

Add to CiteULike CiteULike   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?



This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
dc07-0140v1
30/8/2034    most recent
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Rigalleau, V.
Right arrow Articles by Gin, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Rigalleau, V.
Right arrow Articles by Gin, H.
Social Bookmarking
Add to CiteULike   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Diabetes Diabetes Care Clinical Diabetes Diabetes Spectrum