Saudi Journal of Kidney Diseases and Transplantation

: 2011  |  Volume : 22  |  Issue : 2  |  Page : 286--290

Prevalence of anemia in type 2 diabetes and role of renal involvement

Shokoufeh Bonakdaran, Mohammad Gharebaghi, Mohammad Vahedian 
 Endocrine Research Center, Faculty of Medicine, Ghaem Hospital, Mashhad University of Medical Sciences, Mashhad, Iran

Correspondence Address:
Shokoufeh Bonakdaran
Endocrine Research Center, Faculty of Medicine, Ghaem Hospital, Mashhad University of Medical Sciences, Postal Code 91766, Mashhad


Anemia is more common and more severe in diabetics compared to nondiabetic chronic kidney disease patients. This study was undertaken to determine the prevalence of anemia and the contribution of level of nephropathy to anemia in type 2 diabetic patients. A total of 1,962 patients with type 2 diabetes were evaluated for anemia and biochemical profile. 19.6% of the pa­tients had anemia. 38.1% of patients had albuminuria, 8.1% had moderate (creatinine clearance (CrCl) <60 mL/min/1.73 m 2 ) and 31.4% had mild (CrCl = 60-90 mL/min) renal impairment. Dia­betic patients with moderate renal impairment had significantly more anemia than diabetics with mild renal failure (30% vs. 9%, P = 0.000 Albuminuria was also associated with anemia (8.4% vs. 5.7%, P = 0.000). Cardiovascular disease and retinopathy were also more frequent in diabetic patients with anemia (P = 0.01 and 0.001, respectively). In conclusion, anemia is a highly prevalent finding in Iranian type 2 diabetic patients. Any degree of renal impairment and albumi­uria are the greatest risk factors for anemia in these patients.

How to cite this article:
Bonakdaran S, Gharebaghi M, Vahedian M. Prevalence of anemia in type 2 diabetes and role of renal involvement.Saudi J Kidney Dis Transpl 2011;22:286-290

How to cite this URL:
Bonakdaran S, Gharebaghi M, Vahedian M. Prevalence of anemia in type 2 diabetes and role of renal involvement. Saudi J Kidney Dis Transpl [serial online] 2011 [cited 2019 Dec 9 ];22:286-290
Available from:

Full Text


Diabetes mellitus (DM) is a common meta­bolic disease. [1] Anemia is more frequent and more severe at any level of glomerular filtration rate (GFR) in diabetics compared to nondia­betic patients. [2],[3],[4],[5],[6] The pathogenesis of anemia in diabetes includes deficiency in erythropoietin synthesis and release, systemic inflammation, iron deficiency and probably iatrogenic factors, e.g., angiotensin converting enzyme (ACE) in­hibitors. Anemia is associated with a more ra­pid decline in the GFR and is considered to be an important cardiovascular risk factor. [3],[4],[5] It is therefore important to diagnose and correct ane­mia. The aim of this study was to determine the prevalence of anemia in type 2 diabetics and to assess its association with other variables.

 Subjects and Methods

A total of 1,962 type 2 diabetic patients fol­lowed up in an outpatient clinic were selected. The majority of patients were referred by ge­neral practitioners. All the patients gave in­formed voluntary consent, and the protocol was approved by the local ethics committee. Va­riables were measured from the second routine clinical visit, including creatinine, blood urea nitrogen, fasting blood glucose, HbA1C, lipid profile, uric acid, urinary albumin to creatinine ratio of morning spot urine sample, which were all measured in the same laboratory. Clinical data including anthropometric measurement, age, gender, body mass index, duration of dia­betes, blood pressure, history of ACE inhibitor usage and the presence or absence of cardio­vascular disease and retinopathy were obtained from records and examination by a specialist. Hemoglobin (Hb) concentration and its indexes were obtained for all the patients. The pre­sence of anemia was defined by a Hb <130 g/L in men and <120 g/L in women on the basis of definition of WHO. [7] Patients with iron defi­ciency anemia and thalassemia based on mean corpuscular volume (MCV) iron and total iron binding capacity (TIBC) levels and with other systemic disorders that could result in anemia were excluded from the study. Albumin excre­tion was determined by calculation of albumin to creatinine ratio in spot urine test done in fresh early morning sample. Microalbuminuria was defined as this ratio between 30 and 300 mg/g and macroalbuminuria was defined as more than 300 mg/g in two of three measure­ments. [8] Creatinine clearance (CrCl) was mea­sured using the Cockcroft-Gault formula. Nor­mal renal function was defined by CrCl >90 mL/min/1.73 m 2 , moderate renal impairment by CrCl <60 mL/min/1.73 m 2 and mild renal impairment by a CrCl between 60 and 90 mL/ min/1.73 m 2 . Presence of metabolic syndrome was defined according to ATPIII criteria. Fas­ting plasma glucose was measured by the glucose oxidase method (Human, Heidelberg Germany). Total cholesterol, triglyceride and high density lipoprotein (HDL) were measured by enzymatic method (Parsazmon, Karaj, Iran). Low density lipoprotein (LDL) was calculated according to Friedewald formula (LDL= total cholesterol - (HDL + TG/5). Glycated hemo­globin A1C was assessed by column chromato­graphy (Biosource kit, Barcelona, Spain). Urine albumin in spot urine was measured by immu­noturbidometry assay (Parsazmon, Karaj, Iran). Urine creatinine was measured by enzymatic colorimetric assay and the urine albumin to creatinine ratio was used. Statistical analyses were performed using SPSS version 11.5. Data were expressed as mean ± SD. Variants that failed the normality test were calculated by Mann-Whitney test. Other variables were tes­ted by either one-way or Student's "?" test. Ca­tegorical variables were compared by Chi­square test. Pearson correlation coefficient and Spearman correlation coefficient were com­pared to quantify the correlation of anemia and other variants. A P value <0.05 was considered significant. Logistic analysis was used for the analysis of associations between independent predictors.


Clinical characteristics of patients are shown in [Table 1]. In all patients, the prevalence of anemia was 19.6% and had an equal gender distribution. Prevalence of albuminuria (micro or macro) was 38.1% in all patients. 8.1% of our patients had moderate and 31.4% had mild renal impairment. Among the patients over the age 65 years, 71.8% had evidence of renal im­pairment (mild or moderate), but in patients under the age of 65 years, about 30% had renal impairment (P = 0.000). Also, prevalence of al­buminuria increased with advancing age. A sig­nificant association was found between CrC1 and the prevalence of anemia. Patients with diabetes and moderate renal impairment had significantly more anemia than patients with mild renal involvement (30% vs. 9%, P = 0.000) and normal renal function (30% vs. 7.2%, P = 0.000). Patients with mild renal impairment (CrC1 between 60 and 90) mL/min had sig­nificantly more anemia than normal GFR (9% vs. 7.2%, P = 0.000). Patients with albumi­nuria (micro or macro) had a greater preva­lence of anemia than patients without albumi­nuria (14.2% vs. 5.7%, P = 0.002). Patients with macroalbuminuria had significantly more anemia than patients with microalbuminuria (32.4% vs. 8.4%, P = 0.000), even after adjusting for the degree of renal impairment. Also, patients with microalbuminuria were more likely to have anemia than patients without elevated albuminuria (8.4% vs. 5.7%, P = 0.000). Females had more anemia than male patients but the difference was not significant (10.4% vs. 9.2%, P = 0.2). Association between the presence of anemia and duration of dia­betes was significant (P = 0.002). Patients with anemia had significantly greater uric acid le­vels than patients without anemia (4.86 vs. 4.53, P = 0.000), but after adjusting for lower CrCl and albuminuria, this result was not ob­served (P = 0.46). The association between ACE inhibitor use and prevalence of anemia was significant (P = 0.001), but after correc­tion for difference in CrCl and elevated albu­minuria, the P value was 0.22. The association of anemia with retinopathy, cardiovascular in­volvement, and hypertension was significant (P = 0.01, 0.001, and 0.001, respectively). The association of other variables with the preva­lence of anemia was not significant [Table 2]. Regression analysis revealed a significant cor­relation between anemia and CrCl and anemia and albuminuria (P = 0.001 and 0.018, respec­tively).{Table 1}{Table 2}


In our study, patients had high prevalence of anemia (19.6%) after excluding iron deficiency anemia and other systemic disorders. Thomas et al reported that 20% of 2,125 type 2 diabetic patients had anemia. [9] Craig et al showed that 17.8% of male type 2 diabetic patients and 11.8% of females were classified as anemic. [10] Tomas et al, [11] in another study on 722 diabetic patients, reported that about 23.3% of all pa­tients had anemia. In the study by Cawood et al, [12] it was reported that 11% of males and 16% of females from 270 type 2 diabetic pa­tients were anemic. Our results, though similar, are significant since we excluded all patients with iron deficiency anemia and other syste­mic disorders. Anemia in our diabetics also correlated significantly with renal insufficiency and presence of albuminuria. In the report by Li veachi et al, [13] anemia is more prevalent in the diabetic patients with CrCl <60 mL/min. In most studies to date, impaired renal function and albuminuria are the predominant risk fac­tors for anemia in diabetic patients. [14],[15] In the present study, we showed an independent association between albuminuria and anemia. Tubulointersitial damage occurs early in the course of diabetes even before any fall in GFR and may be associated with the degree of albu­minuria. [16] Furthermore, systemic inflammation in diabetes is able to reduce the effect of ery­thropoietin (EPO) and it seems that one of the most potent causes of poor response to EPO is chronic inflammation. [15] In the study by Thomas et al, patients with elevated albuminuria had a greater prevalence of anemia. [9] Mojimiyi et al [17] reported that with increasing degree of micro­albuminuria, EPO decreased more and a sig­nificant correlation was found between albumin- creatinine ratio and log of EPO, and it was shown that the most significant marker of EPO deficiency was the degree of albuminuria. We did not study EPO levels in our patients but our findings are in agreement with other studies that showed increased frequency of anemia in albuminuric diabetic patients. A strong asso­ciation between urine albumin to creatinine ratio and low Hb levels suggests that the evol­ving nephropathy probably plays a similar role to overt renal dysfunction. This may be due to the predominance of injury to cells and vas­cular component of the renal tubulointersti­tium associated with diabetic nephropathy that may be apparent, like albuminuria. We found a significant association between ACE inhibitor usage and anemia, but after adjustment for CrCl, this association was not significant. Another study [18] also does not support any significant correlation between ACE inhibitor use and anemia. We found significant comorbidities such as cardiovascular disease, retinopathy and hypertension, which may be related to duration of diabetes, renal impairment and albuminuria itself. However, some of the effects of renal impairment, especially cardiovascular compli­cations, may be mediated through anemia. [19],[20],[21],[22] Anemia due to hypoxia increases the oxidative stress, thus enhancing neo-vascularization in diabetic patients and leading to tissue edema. [23]

In conclusion, anemia is prevalent in type 2 diabetics especially with renal impairment and is a significant risk factor for diabetic compli­cations. Correction of anemia may have a sig­ nificant role in prevention of other diabetic complications.


1US Renal Data System. USRDS 2002. Annual data report. National institutes of health, National institute of Diabetes and digestive and kidney diseases 2001.
2Thomas MC, Macisaac RJ, Tsalamandris C, Power D, Jerums G. Unrecognized anaemia in patients with diabetes. Diabetes Care 2002;24: 1164-9.
3Astor BC, Muntner P, Levin A, Eustace JA, Coresh J. Association of kidney function with anaemia: the Third National Health and Nutri­tion Examination Survey (1988-94). Arch Intern Med 2002;162:1401-8.
4Dikow R, Schwenger V, Schomig M, Ritz E. How should we manage anaemia in patients with diabetes? Nephrol Dial Transplant 2001; 17:67-72.
5Bosman DR, Winker AS, Marseden JT, Mac­Dougall IC, Watkins PJ. Anaemia with ery­thropoietin deficiency occurs early in diabetic nephropathy. Diabetes Care 2002;24:495-9.
6Deray G, Heurtier A, Grimaldi A. Anemia and diabetes. Am J Nephrol 2004;24:522-6.
7World Health Organization. Nutritional Anaemia. Report of a WHO scientific group. WHO, Geneva, 1968
8Brownlee M, Aiello L, Cooper M, Vinik AI, Nesto RW, Boulton A. Complication of dia­betes mellitus. In: Kronerberg H, Melmod SH, Polonsky K, Larsen P. Williams Textbook of Endocrinology. 11nd ed. Saunders 2008;1445.
9Thomas MC, MacIsaac RJ, Tsalamandris C, et al. The burden of anaemia in type 2 diabetes and the role of nephropathy: a cross- sectional audit. Nephrol Dial Transplant 2004;19:1792-­7.
10Griac K, Williams JD, Riley SG, et al. Anemia and diabetes in the absence of nephropathy 2005;28:1118-23.
11Thomas MC, Cooper ME, Tsalamandris C, Maclsaac R, Jerums G. Anemia with impaired erythropoietin response in diabetic patients. Arch Intern Med 2005;165:466-9.
12Cawood TJ, Buckley U, Murray A, et al. Pre­valence of anaemia in patients with diabetes mellitus. Ir J Med Sci 2006;175:25-7.
13Li Vecchi M, Fuiano G, Francesco M, et al. Prevalence and severity of anaemia in patients with type 2 diabetic nephropathy and different degrees of chronic renal insufficiency. Nephron Clin Prac 2007;105:62-7.
14Thomas MC, Macisaac RJ, Tsalamandris C, et al. Anemia in patients with type 1 diabetes. J Clin Endocrinol Metab 2004;89:4359-63.
15Fioretto P, Mauer M, Brocco E, et al. Patterns of renal injury in NIDDM patients with micro­albuminuria. Diabetologia 1996;39:1569-76.
16Brito PL, Fioretto P, Drummond K. Proximal tubular basement membrane width in insulin dependent diabetes mellitus. Kidney Int 1998; 53:574-61.
17Mojiminiyi OA, Abdella NA, Zakit MY, Gebely AE, Mohamedi HM, Aldhahi W. Prevalence and association of low plasma erythropoietin in patients with type 2 diabetes mellitus. Diabet Med 2006;23:839-44.
18Hayashi K, Hasegawa K, Kobayashi S. Effects of angiotensin-converting enzyme inhibitors on the treatment of anaemia with erythropoietin. Kidney Int 2001;60:1910-6.
19AL-Ahmad A, Rand W, Majunath G, et al. Reduced Kidney function and anemia as a risk factors for mortality in patients with left ven­tricular dysfunction. J Am Coll Cardiol 2001, 38:955-62.
20Zeidman A, Fradin Z, Blecher A, Oster HS, Avrahami Y, Mittelman M. Anemia as a risk factor ischemic heart disease. Isr Med Assoc J 2004;6:16-8.
21Nikolsky E, Aymong ED, Halkin A, et al. Impact of anemia in patients with acute myocardial infarction undergoing primary percutaneous coronary interventions. Analysis from the con­trolled abciximab and device investigation to lower late angioplasty complications trial. J Am Coll Cardiol 2004;44:547-53.
22Lee PC, Kini AS, Ahsan C. Anemia is an inde­pendent predictors of mortality after percuta­neous coronary intervention. J Am Coll Cardiol 2004;44:541-6.
23Thomas M, Tsalamandris C, MacIsaac R, Jermus G. Anaemia in diabetes: an emerging compli­cation of microvascular disease. Curr Diabetes Rev 2005;1:107-26.