RENAL DATA FROM THE ARAB WORLD
|Year : 2015 | Volume
| Issue : 5 | Page : 1035-1043
|Diabetic kidney disease and vascular comorbidities in patients with type 2 diabetes mellitus in a developing country
Yassamine Bentata1, A Chemlal1, I Karimi1, F El Alaoui1, I Haddiya1, Redouane Abouqal2
1 Department of Nephrology, Medical School of Oujda, University Mohamed the First, Oujda, Morocco
2 Department of Medical Emergency, Ibn Sina University Hospital; Department of Epidemiology, Laboratory of Biostatistics, Clinical and Epidemiological Research, Medical School University Mohamed V Souissi, Rabat, Morocco
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|Date of Web Publication||7-Sep-2015|
| Abstract|| |
Type 2 diabetes mellitus (T2DM) is associated with an increased risk of progression toward end-stage renal disease and cardiovascular (CV) risk mortality. To investigate this association, we studied 637 patients with T2DM in the Eastern area of Morocco. The mean follow-up period was 42 ± 11 months. At the baseline visit, 22.8%, 59.1% and 18.1% of the patients had normo-albuminuria, micro-albuminuria and macro-albuminuria, respectively. Of all patients, 51.6% had a history of hypertension and 37.4% had hypertension on admission. At the end of follow-up, rapid progression (estimated glomerular filtration rate >5 mL/min/1.73 m 2 /year) was observed in 24.1% of the cases and the frequency of occurrence of CV events was 5%, 18.5% and 32.5% in the normo-, micro- and macro-albuminuria groups, respectively (P <0.001). In multivariate analysis, arterial hypertension was identified as an independent risk factor related to diabetic kidney disease (DKD, P = 0.04) and occurrence of CV events (P = 0.02), while albuminuria was not identified as an independent risk factor, either for DKD or for the occurrence of CV events. Our study found that hypertension was an independent risk factor for the DKD and the occurrence of the CV events in T2DM patients.
|How to cite this article:|
Bentata Y, Chemlal A, Karimi I, El Alaoui F, Haddiya I, Abouqal R. Diabetic kidney disease and vascular comorbidities in patients with type 2 diabetes mellitus in a developing country. Saudi J Kidney Dis Transpl 2015;26:1035-43
|How to cite this URL:|
Bentata Y, Chemlal A, Karimi I, El Alaoui F, Haddiya I, Abouqal R. Diabetic kidney disease and vascular comorbidities in patients with type 2 diabetes mellitus in a developing country. Saudi J Kidney Dis Transpl [serial online] 2015 [cited 2022 Jul 7];26:1035-43. Available from: https://www.sjkdt.org/text.asp?2015/26/5/1035/164602
| Introduction|| |
In type 2 diabetes mellitus (T2DM), 40-50% of patients develop microand macro-albuminuria. , The natural history of diabetic kidney diseases (DKDs) consists of progression from micro-albuminuria to macro-albuminuria and overt proteinuria.  An increase in the albumin excretion rate (AER) is considered as an early marker of DKD, while renal impairment, defined as estimated glomerular filtration rate (eGFR) <60 mL/min/1.73 m 2 , generally occurs only several years after the beginning of overt proteinuria.  However, not all T2DM patients with renal impairment have albuminuria and nearly 50% of patients with T2DM develop normo-albuminuric renal impairment. ,, Fifty percent to 93% of T2DM patients have arterial hypertension, regardless of the AER. ,, Albuminuria is also a strong marker for cardiovascular (CV) events as it represents diffused endothelial dysfunction in T2DM. ,
In T2DM, hypertension is another strong risk factor for CV disease, and up to 75% of specific CV complications are attributable to hypertension. , Additionally, hypertension is a major causal factor of end-stage kidney failure in T2DM. ,
The aim of the present study was to investigate the association between albuminuria, hypertension, eGFR and CV events in a prospective cohort of T2DM patients in a developing country.
| Materials and Methods|| |
This is a prospective study and was conducted at the Reference Center for Chronic Diseases in Oujda, Morocco (Eastern Morocco, North Africa) that was started in September 2006. The Ethics Committee of Morocco's Mohammed V University in Rabat approved the study protocol (University Mohamed V Souissi, Rabat). Informed consent was obtained from all participants.
The inclusion criteria included patients who were >20 years of age with confirmed T2DM, had newly diagnosed kidney disease (<6 months) and who were regularly followed in nephrology consultation. TD2M was confirmed according to the World Health Organization (WHO) criteria. 
Excluded from the study were T2DM patients who were pregnant during the follow-up, had a single kidney or a pathology other than diabetes and hypertension capable of altering renal function (renal lithiases, current urinary infection, polycystic kidney disease, a neoplasm, long-term use of nephrotoxic medications), had end-stage renal disease on admission, did not have clinical and biological parameters available at the time of enrolment or during follow-up, had follow-up of <24 months or were of black race. Patients who used angiotensin-converting enzyme inhibitors (ACEi) or angiotensin receptors blockers (ARBs) before the onset of the study were also excluded as well were patients with type 1 diabetes.
We calculated the eGFR with the abbreviated Modification of Diet in Renal Disease (MDRD) Study equation. We used in the measurement of creatinine the calibrated Jaffe method and not the isotope dilution mass spectrometry because it is expensive and not available in our country, and we reduced the creatinine concentrations by 5% as previously reported. 
To determine the micro-albuminuria, we used the conventional immunoturbidimetric assay and we considered an AER to be positive when it was positive in three specimens without any treatment based on ACEi or ARBs and independently of any concomitant urinary infection, fever and/or menstrual cycle.
The clinical and biological parameters were collected at the time of enrolment, each year and at the end of the follow-up for each patient.
We defined hypertension as systolic blood pressure of at least 140 mm Hg, diastolic blood pressure of at least 90 mm Hg or use of antihypertensive drugs. Body mass index (BMI) was calculated by dividing body weight (kg) by the squared height (kg/m 2 . The study population was divided into three groups: normoalbuminuria (AER <30 mg/day) micro-albuminuria (AER = 30-299 mg/day) or macroalbuminuria (AER ≥300 mg/day) based on 24h urine collection.
We defined renal impairment as eGFR <60 mL/min/1.73 m 2 for at least three months , and independence of any other pathology other than diabetes and arterial hypertension that might explain this renal impairment.
The presence of diabetic retinopathy was assessed by dilated fundoscopy.
The patients were monitored for the presence or absence of vascular co-morbidities such as ischemic heart disease (history of angina, myocardial infarction, heart failure and/or coronary revascularization) and/or peripheral vascular disease (amputation and/or gangrene of the lower limbs) and/or cerebrovascular disease (history of stroke).
| Statistical analysis|| |
Quantitative variables were expressed as mean ± standard deviation or as median and interquartile range following their distribution. Qualitative variables were expressed as frequency and percentage. Comparison of quantitative variables between the three groups was performed by using the analysis of variance (ANOVA) test in case of variables that showed symmetrical distribution or by the Kruskal-Wallis test in case of variables that showed asymmetrical distribution. The comparison of qualitative variables between the three study groups was performed using the Chi square test. Associations between the eGFR and covariates of interest were investigated using univariate and multivariate binary logistic regression with the proportional odds ratio. A two-tailed P-value <0.05 was considered significant. All the statistical analyses were carried out using SPSS for Windows 13.0 (SPSS Inc., Chicago, IL, USA).
| Results|| |
Among the 2156 T2DM patients referred for nephrology consultation, only 637 patients met the inclusion criteria. The mean age of the patients was 58.5 ± 10.8 years (ranging from 31 to 91 years); 29.2% of them were over 65 years of age and 8.3% were under 45 years of age, and the sex ratio was 0.60. Morbid obesity was observed in 5.3% of the cases. At the baseline visit, 22.8%, 59.1% and 18.1% of the patients had normo-albuminuria, micro-albuminuria and macro-albuminuria, respectively. Of all the patients, 51.6% had a history of hypertension and 37.4% had hypertension on admission, including 15.5% diagnosed at the time of enrolment. Normo-albuminuria renal impairment was observed in 6.2% of all patients. Among patients with hypertension history, 62.6% and 22.8% had micro and macro-albuminuria, respectively, vs 55.5% and 13% (P <0.001) among patients without hypertension history. Among patients with a history of hypertension, 28.6% had renal impairment vs 14.6% among patients without a history of hypertension (P <0.001). Among patients with a history of hypertension, 9.3% were smokers vs 14.4% among patients without a history of hypertension (P = 0.05). Among patients with a history of hypertension, 16.7% also had a history of CV comorbidities vs. 8.1% among patients with no history of hypertension (P = 0.001). [Table 1] shows the clinical and biological parameters of all the patients and a comparison of parameters between the three groups of patients at the time of enrolment.
|Table 1: Clinical and biological characteristics of all patients and a comparison of parameters between the three groups of patients at the time of enrolment.|
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The mean follow-up period was 42 ± 11 months. [Table 2] shows the clinical and biological parameters of all patients and a comparison of parameters between the three groups at the end of follow-up. Revascularization by cardiac angioplasty with insertion of stent and/ or coronary bypass surgery was found in 12.3% of patients who presented ischemic heart disease during the follow-up. There were 33.6% of patients who had hypertension at the end of follow-up vs 37.4% at the time of enrollment. Among patients with a history of hypertension, 60.8% had hypertension at the time of enrolment vs. 45.3% at the end of follow-up (P <0.001), with the use of more than two antihypertensive drugs in 52.9% of cases at the end of follow-up. Among patients who had no known history of hypertension, 12.3% had hypertension at the time of enrolment vs. 21.1% at the end of follow-up (P <0.001), with the use of more than two antihypertensive drugs in 11.4% of the cases at the end of follow-up.
|Table 2: Clinical and biological characteristics of all patients and a comparison of parameters between the three groups of patients at the end of follow-up.|
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We observed a resolution of micro-albuminuria in 18.5% of the cases and of macroalbuminuria in 1.7% of the cases, a regression from macro-albuminuria toward micro-albuminuria in 33% of the cases, a progression from normo-albuminuria toward micro-albuminuria in 15.8% of the cases and from microalbuminuria toward macro-albuminuria in 5.8% of the cases. No case of passage from normo-albuminuria toward macro-albuminuria was observed; 35.6% of the patients with macro-albuminuria had albuminuria of between 300 and 500 mg/day.
At the end of follow-up, 30.1% of the patients with history of hypertension had renal impairment vs. 15.2% among patients without history of hypertension (P <0.001). The mean age was 57 ± 10 years in the group that maintained an eGFR >60 mL/min/1.73 m 2 vs. 63 ± 9 years in the group that developed an eGFR <60 mL/min/1.73 m 2 (P <0.001).
The frequency of the CV events was higher in the group with a history of hypertension, 19.5% vs. 8.4% in the group without a history of hypertension (P <0.001).
While analyzing the progression factors for DKD in T2DM, we found in the univariate analysis that advanced age, duration of diabetes, diabetic retinopathy, diabetic neuropathy, history of vascular comorbidities, history of hypertension, baseline albuminuria, reduced baseline eGFR, low baseline hemoglobin and elevated baseline HbA1c were associated with a decline of eGFR. In multivariate analysis, advanced age, hypertension and low baseline eGFR were identified as independent risk factors for a decline of eGFR. Albuminuria was not retained as an independent risk factor for a decline of eGFR in our study.
In analyzing the factors for occurrence of CV events in T2DM, we found in the univariate analysis that the duration of diabetes, diabetic retinopathy, diabetic neuropathy, history of vascular comorbidities, history of hypertension, smoking, BMI, baseline albuminuria, reduced baseline eGFR, and low baseline hemoglobin were associated with high occurrence of CV events. In the multivariate analysis, only smoking, history of hypertension, history of vascular comorbidities and obesity were identified as independent risk factors for the occurrence of CV events. Albuminuria was not identified as an independent risk factor for the occurrence of CV events.
| Discussion|| |
In our study, the prevalence of microand macro-albuminuria was 59.1% and 18.1%, respectively, among T2DM patients. This high percentage can be explained by the fact that the study involved T2DM patients referred for specialized nephrology consultation for treatment of a recently diagnosed DKD and/or arterial hypertension. All published studies report clinical and biological data of T2DM patients from primary care centers, whereas our study was conducted within the nephrology care centers. At the level of primary care centers, the prevalence of micro-albuminuria among T2DM patients is quite low. It was 20.6% in an Iranian series, 16.4% in a Swedish study, 26% in an Italian series, 28.8% in a Belgian series, 32% in a series from three Gulf countries (United Arab Emirates, Bahrain and Oman) and 13% and 19.5% in two Spanish series. ,,,,,, The global DEMAND study stated that the overall prevalence of micro-albuminuria among T2DM patients was 39% and the DEMAND Asian study reported the prevalence at 44%. , However, the prevalence of macro-albuminuria was 5.1%, 5.4%, 9.3%, 2.3% and 4%, respectively, in the Iranian, Italian, Belgian and Spanish series. ,,, In the global DEMAND study, the overall prevalence of macro-albuminuria was 10%, while it was 12% in the Asian DEMAND study and 3.5% in the Italian DEMAND study. , Ethnicity may explain these wide variations of incidence. The frequency of T2DM patients with normo-albuminuric renal impairment is increasingly high; 56.6% of the patients were normo-albuminuric with reduced eGFR in an Italian multicenter study.  Although the use of inhibitors of the angiotensin-renin system partly explains this DKD picture, other factors such as sex and age may play an important role in the pathophysiological mechanism.  The regression of micro-albuminuria is classic in T2DM, but regression of macro-albuminuria to microor normo-albuminuria is rare. In our study, the rate of regression of macroalbuminuria to the stage of micro-albuminuria was observed in 33% of the cases, which may be explained on the one hand by optimization of the prescription of ACEi and ARBs, 81.5% of patients taking ACEi or ARBs at the end of follow-up, and on the other hand by the fact that 36.5% of patients with macro-albuminuria had an AER of <500 mg/day.
Albuminuria was not found as an independent risk factor for decline of eGFR in our study. This is probably related to the fact that 77.2% of our patients had albuminuria at admission, contrary to other studies where less than one-third of patients presented albuminuria. ,,,,,,
Hypertension was found as an independent factor of DKD progression in our study, underlining the major role played by hypertension. Indeed, the patients with T2DM and hypertension have a seven-fold greater risk for progression to end-stage renal failure.  In the cohort of Lou et al, hypertension was found to be an independent risk factor in multivariate analysis of progression of chronic kidney disease in Chinese patients with T2DM. 
In our study, multivariate analysis did not identify albuminuria as an independent risk factor for the occurrence of CV events. Other studies confirm that coronary events were more strongly associated with normo-albuminuric renal impairment than albuminuric renal impairment. , This is in marked contradiction with the earlier concept according to which albuminuria is a powerful predictive factor for coronary events. ,,, Has the reduction of albuminuria with the ACEi or ARBs reversed the link between albuminuria and CV events? More studies are warranted to substantiate our findings.
Arterial hypertension remains an independent risk factor for the occurrence of CV events, and it is well established that patients with T2DM have a twoto four-fold greater risk for developing CV sequalae as compared with age-matched control subjects and with patients having T2DM and normal blood pressure. , This is especially true given that blood pressure objectives are difficult to attain and a great many T2DM patients remain hypertensive under treatment. We also identified obesity as an independent risk factor for the occurrence of CV events. Nevertheless, the results of published studies concerning the link between obesity and CV risk in T2DM patients remain inconclusive. Some studies identify BMI as a risk factor for CV events in T2DM. , Other studies however do not confirm the role of BMI in the occurrence of CV events. 
There were several limitations in our study. First, we used the MDRD to estimate GFR rather than the measurement of GFR using iothalamate clearance to determine kidney function. Secondly, we identified CV events using clinical criteria only; we did not carry out systematic examinations to detect CV disease. Thirdly, we were unable to optimize the control of patients' clinical and biological parameters during follow-up as our patients were financially unable to buy the necessary medications because of their low socioeconomic level and the lack of medical insurance.
The strengths of this study are as follows. First, it was conducted within a nephrology department that evaluated the progression of eGFR and the occurrence of CV events among patients with T2DM who had an increased incidence of microand macro-albuminuria at the time of enrolment in the study. Second, albuminuria was confirmed in three urine samples, which leaves no room for doubt as to the stage of albuminuria. Third, the patients had not received any treatment based on ACEi or ARBs before the beginning of the study, which means that the stage of albuminuria identified at the start of the study was not influenced by interventions.
In conclusion, our study demonstrated that hypertension was an independent risk factor of DKD and of the occurrence of CV events, while albuminuria was not identified as an independent risk factor, either for DKD or for the occurrence of CV events. This shows the benefit of early detection of hypertension and of intensifying our efforts to ensure optimal control of blood pressure during our follow-up of T2DM patients. Moreover, other studies with more rigorous inclusion criteria and strict methodology are needed in order to accurately study the link between albuminuria, hypertension, eGFR and CV risk in T2DM.
Conflict of Interest
The authors declare that they have no conflicts of interest concerning this article.
| References|| |
Parving HH, Lewis JB, Ravid M, Remuzzi G, Hunsicker LG; DEMAND investigators. Prevalence and risk factors for microalbuminuria in a referred cohort of type II diabetic patients: A global perspective. Kidney Int 2006;69:2057-63.
Koro CE, Lee BH, Bowlin SJ. Antidiabetic medication use and prevalence of chronic kidney disease among patients with type 2 diabetes mellitus in the United States. Clin Ther 2009;31:2608-17.
Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmanovitz T. Diabetic nephropathy: Diagnosis, prevention, and treatment. Diabetes Care 2005;28:164-76.
National Kidney Foundation. K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Am J Kidney Dis 2002;39 2 Suppl 1:S1-266.
Kramer HJ, Nguyen QD, Curhan G, Hsu C. Renal insufficiency in the absence of albuminuria and retinopathy among adults with type 2 diabetes mellitus. J Am Med Assoc 2003;289:3273-7.
Thomas MC, Macisaac RJ, Jerums G, et al. Nonalbuminuric renal impairment in type 2 diabetic patients and in the general population (national evaluation of the frequency of renal impairment co-existing with NIDDM [NEFRON] 11). Diabetes Care 2009;32:1497-502.
Ito H, Takeuchi Y, Ishida H, et al. High frequencies of diabetic microand macroangiopathies in patients with type 2 diabetes mellitus with decreased estimated glomerular filtration rate and normoalbuminuria. Nephrol Dial Transplant 2010;25:1161-7.
Coll-de-Tuero G, Mata-Cases M, RodriguezPoncelas A, et al. Chronic kidney disease in the type 2 diabetic patients: Prevalence and associated variables in a random sample of 2642 patients of a Mediterranean area. BMC Nephrol 2012;13:87.
Rodriguez-Poncelas A, Garre-Olmo J, Franch-Nadal J, et al. Prevalence of chronic kidney disease in patients with type 2 diabetes in Spain: PERCEDIME2 study. BMC Nephrol 2013;14:46.
Viana LV, Gross JL, Camargo JL, Zelmanovitz T, da Costa Rocha EP, Azevedo MJ. Prediction of cardiovascular events, diabetic nephropathy, and mortality by albumin concentration in a spot urine sample in patients with type 2 diabetes. J Diabetes Complications 2012;26:407-12.
Gerstein HC, Mann JF, Yi Q, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 2001;286:421-6.
Arnlöv J, Evans JC, Meigs JB, et al. Lowgrade albuminuria and incidence of cardiovascular disease events in nonhypertensive and nondiabetic individuals: The Framingham Heart Study. Circulation 2005;112:969-75.
Sowers JR, Epstein M, Frohlich ED. Diabetes, hypertension, and cardiovascular disease: An update. Hypertension 2001;37:1053-9.
Campbell NR, Leiter LA, Larochelle P, et al. Hypertension in diabetes: A call to action. Can J Cardiol 2009;25:299-302.
Bild D, Teutsch SM. The control of hypertension in persons with diabetes: A public health approach. Public Health Rep 1987;102:522-9.
Perneger TV, Brancati FL, Whelton PK, Klag MJ. End-stage renal disease attributable to diabetes mellitus. Ann Intern Med 1994;121:912-8.
Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: Diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 1998;15:539-53.
Levey AS, Coresh J, Greene T, et al. Expressing the Modification of Diet in Renal Disease Study equation for estimating glomerular filtration rate with standardized serum creatinine values. Clin Chem 2007;53:766-72.
National Kidney Foundation. KDOQI clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease. Am J Kidney Dis 2012;60(5): 850-86.
Levey AS, Coresh J, Balk E, et al. National Kidney Foundation practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Ann Intern Med 2003;139:137-47.
Zakkerkish M, Shahbazian HB, Shahbazian H, Latifi SM, Moravej Aleali A. Albuminuria and its correlates in type 2 diabetic patients. Iran J Kidney Dis 2013;7:268-76.
Sjöblom P, Nystrom FH, Länne T, Engvall J, Östgren CJ. Microalbuminuria, but not reduced eGFR, is associated with cardiovascular subclinical organ damage in type 2 diabetes. Diabetes Metab 2014;40:49-55.
Targher G, Zoppini G, Chonchol M, et al. Glomerular filtration rate, albuminuria and risk of cardiovascular and all-cause mortality in type 2 diabetic individuals. Nutr Metab Cardiovasc Dis 2011;21:294-301.
Doggen K, Nobels F, Scheen AJ, Van Crombrugge P, Van Casteren V, Mathieu C. Cardiovascular risk factors and complications associated with albuminuria and impaired renal function in insulin-treated diabetes. J Diabetes Complications 2013;27:370-5.
Prashanth P, Sulaiman KJ, Kadaha G, et al. Prevalence and risk factors for albuminuria among type 2 diabetes mellitus patients: A Middle-East perspective. Diabetes Res Clin Pract 2010;88:e24-7.
Pan CY, Ho LT, Soegondo S, et al. Prevalence of albuminuria and cardiovascular risk profile in a referred cohort of patients with type 2 diabetes: An Asian perspective. Diabetes Technol Ther 2008;10:397-403.
Pugliese G, Solini A, Bonora E, et al. Chronic kidney disease in type 2 diabetes: Lessons from the renal insufficiency and cardiovascular events (RIACE) Italian multicentre study. Nutr Metab Cardiovasc Dis 2014;24:815-22.
Penno G, Solini A, Bonora E, et al. Clinical significance of nonalbuminuric renal impairment in type 2 diabetes. J Hypertens 2011;29:1802-9.
Lou QL, Ouyang XJ, Gu LB, et al. Chronic kidney disease and associated cardiovascular risk factors in Chinese with T2 diabetes. Diabetes Metab J 2012;36:433-42.
Penno G, Solini A, Zoppini G, et al. Rate and determinants of association between advanced retinopathy and chronic kidney disease in patients with type 2 diabetes: The renal insufficiency and cardiovascular events (RIACE) Italian multicenter study. Diabetes Care 2012;35:2317-23.
Ninomiya T, Perkovic V, de Galan BE, et al. Albuminuria and kidney function independently predict cardiovascular and renal outcomes in diabetes. J Am Soc Nephrol 2009;20:1813-21.
Drury PL, Ting R, Zannino D, et al. Estimated glomerular filtration rate and albuminuria are independent predictors of cardiovascular events and death in type 2 diabetes mellitus: The Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study. Diabetologia 2011;54:32-43.
Svensson MK, Cederholm J, Eliasson B, Zethelius B, Gudbjörnsdottir S; Swedish National Diabetes Register. Albuminuria and renal function as predictors of cardiovascular events and mortality in a general population of patients with type 2 diabetes: A nationwide observational study from the Swedish National Diabetes Register. Diab Vascu Dis Res 2013;10:520-9.
Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: Epidemiology, pathophysiology, and management. JAMA 2002;287:2570-81.
Stamler J, Vaccaro O, Neaton JD, Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 1993;16:434-44.
Babayev R, Whaley-Connell A, Kshirsagar A, et al. Association of race and body mass index with ESRD and mortality in CKD stages 3-4: Results from the Kidney Early Evaluation Program (KEEP). Am J Kidney Dis 2013;61:404-12.
Fox CS, Matsushita K, Woodward M, et al. Associations of kidney disease measures with mortality and end-stage renal disease in individuals with and without diabetes: A metaanalysis. Lancet 2012;380:1662-73.
Department of Nephrology, Medical School of Oujda, University Mohamed the First, Oujda
Source of Support: None, Conflict of Interest: None
[Table 1], [Table 2]
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