Prevalence of Microalbuminuria Among Patients with Type 2 Diabetes Mellitus

Abstract

Background:

Asian ethnicity is said to be a risk factor for microalbuminuria. Prevalence studies in native Asians, especially Indians, are scarce. The aim was to study the prevalence of microalbuminuria in patients with type 2 diabetes mellitus and to identify the associated risk factors.

Methods:

Eight hundred consecutive patients attending the endocrine outpatient clinic were screened. Six hundred seventy patients were eligible for microalbuminuria screening. Urinalysis was done in a random spot urine sample using dipsticks. History, physical examination, and metabolic data were recorded.

Results:

The mean age and body mass index of the study population were 52.13 ± 9.9 years and 26.19 ± 4.34 kg/m², respectively. The median duration of diabetes was 5 years. Microalbuminuria was found in 25.5% (95% confidence interval, 22.4–29%) and macroproteinuria in 16.2% (95% confidence interval, 13.5–19.1%). In patients with duration of diabetes less than 1 year, the prevalence of microalbuminuria was 24.7%, and that of macroproteinuria was 6.2%. The risk factors associated with microalbuminuria and macroproteinuria were glycated hemoglobin, retinopathy, and calcium channel blocker intake. However, waist circumference was negatively associated with macroproteinuria but not with microalbuminuria. This difference in the risk factors supports the newer concept that microalbuminuria and diabetic nephropathy are pathophysiologically different and may not be inextricably linked.

Conclusions:

The high proportion of patients who present with albuminuria within the first year of diagnosis probably indicates longer duration of prior undiagnosed diabetes. Screening for asymptomatic diabetes and defining newer risk factors to identify those at risk for complications are essential to reduce the socioeconomic burden of diabetes.

Introduction

D iabetes is the single most common cause of end-stage renal disease worldwide and is responsible for huge dialysis costs.¹ With an estimated 40.9 million people with diabetes mellitus (DM), India has the world's largest diabetes population.² Immigrant Asian Indians have been shown to have an increased risk for end-stage diabetic nephropathy.³ In native Indians, 30.3% of the chronic kidney disease is due to diabetic nephropathy.⁴ This highlights the importance of early recognition of diabetic nephropathy, so as to focus on prevention efforts. One such early indicator of diabetic nephropathy is microalbuminuria (MAU).⁵ Besides being a predictor of incipient nephropathy, MAU is also a marker of increased cardiovascular risk.

Epidemiological studies have reported marked variation in the prevalence of MAU, ranging from less than 10% in the United Kingdom⁶ and 23% in Ethiopians⁷ to as high as 35% in Hispanic Americans.⁸ Available literature supports the existence of racial/ethnic variations in the prevalence of MAU.⁹ The variation in the prevalence between different populations may be explained by the differences in study setup, method of urine collection, definition of MAU, estimation of albumin in the urine, etc. Nonetheless, it may reflect a true finding attributable to differences in glycemic control, lifestyle factors, awareness and access to health care, socioeconomic factors, and possibly genetic variations.

High prevalence has been reported in Pima Indians, Mexican Americans, African Americans, and Saudi Arabians.^9,10 Studies from United Kingdom and New Zealand have shown that South Asian immigrants with diabetes are at increased risk for MAU^11

–14 and diabetic nephropathy.¹⁵ Evidence from the United Kingdom Prospective Diabetes Study (UKPDS) also demonstrates that Indian Asian ethnicity is one of the most highly associated risk factor for incident MAU.¹⁶ However, data on prevalence of MAU in native South Asians are scarce. A study from Pakistan reported a prevalence of 34%.¹⁷ There are no published reports from Bangladesh. There are a few reports from South India.^18

–21 There is little information on the prevalence of MAU and the associated risk factors from North India.

The objective of the present study was to assess the prevalence of MAU in patients with type 2 DM and to determine the associated risk factors.

Subjects and Methods

This study was conducted in the endocrine outpatient clinic of a tertiary-care hospital between January 2007 and March 2008. The study protocol was approved by the Institute Ethics Committee. All study subjects gave informed consent for participation in the study.

Subjects

Subjects who were above the age of 18 years and had previously diagnosed type 2 DM were included in the study. Type 2 DM was defined by the World Health Organization study group criteria.²² The following subjects were excluded from the study: (1) those with known diabetic nephropathy/chronic renal failure; (2) those with known urological diseases; (3) those with acute febrile illness; (4) those with congestive heart failure; (5) those with symptomatic urinary tract infection/balanitis/vulvovaginitis; and (6) severe hypertension (blood pressure >170/110 mm Hg) with or without antihypertensive drugs.

Methods

Consecutive patients with type 2 DM attending the clinic who gave informed consent were enrolled. Patients were interviewed in detail regarding onset of diabetes, history of hospitalizations for hyperglycemic crises, history of hypertension, family history of diabetes, and smoking status (nonsmoker or current or former smoker). All documented complications such as retinopathy, cardiovascular disease, and cerebrovascular disease were recorded. All the drugs previously prescribed to the patient were noted.

A complete physical examination was done. Height and weight were measured by standard techniques. Waist and hip circumferences were measured by the method recommended by the World Health Organization in 1995.²³ Blood pressure was recorded in the sitting position in the right arm using a mercury sphygmomanometer. Two readings were taken 10 min apart. The mean of the two was taken as the final blood pressure recording. The latest fasting plasma glucose, glycated hemoglobin (HbA1C), blood urea, and serum creatinine values were noted from the patients' medical record.

A random spot urine specimen was collected, and a colorimetric semiquantitative urine test strip (Combur 10^®, Roche Diagnostics, Mannheim, Germany) was first used to test for pH, specific gravity, leukocytes, nitrite, blood/hemoglobin, and protein. If pH and specific gravity were normal and other parameters were negative, then microalbumin was tested using a dipstick (Micral II^®, Roche Diagnostics). To achieve 95% confidence (CI) with an absolute precision of 3%, a sample size of 800 would be required, assuming a prevalence of 25%.

Definitions

The following definitions were used:

Macroproteinuria: a change in color of the dipstick that corresponded to ≥1+ (30 mg/dL) was considered to be macroproteinuria.²⁴

MAU: a change in the color of the Micral II strip that corresponded to ≥20 mg/L was considered to be positive for MAU.²⁵

Renal failure: individuals with a serum creatinine >1.5 mg/dL were considered to have renal failure and were excluded from the study.

Hypertension: subjects with self-reported hypertension on drugs and those who had a systolic blood pressure of ≥140 mm Hg and/or diastolic blood pressure ≥90 mm Hg were considered to have hypertension.²⁶

Obesity: the classification proposed by the World Health Organization for adult Asians²⁷ was followed, and a body mass index (BMI) of ≥25 kg/m² was considered obesity.

Estimated glomerular filtration rate: the Modification of Diet in Renal Disease (MDRD1) formula was used to estimate glomerular filtration rate.²⁸

Statistical analysis

Data were expressed as mean ± SD values or median (range), as appropriate. Student's t test or the Mann-Whitney U test was used to compare continuous variables, and the χ ² test was used to compare the proportions among different groups. Prevalence was calculated with a two-sided 95% CI.

Multiple logistic regression analysis was performed. In univariate analysis, the link between two variables was considered significant if P < 0.25. The multivariate analysis included only the significant variables. Statistical analyses were performed with SPSS for Windows version 10.0 (SPSS, Inc., Chicago, IL). P < 0.05 was considered statistically significant.

Results

Eight hundred consecutive patients were recruited. On the basis of various exclusion criteria, 105 subjects were excluded: chronic renal failure, 47; acute renal failure, one; glomerular disease, three; polycystic kidney, one; solitary kidney, two; urological disease, 18; symptomatic urinary tract infection, three; vaginitis, two; vesicovaginal fistula, one; uncontrolled blood pressure, two; cardiac disease with congestive cardiac failure, six; chronic liver disease, six; human immunodeficiency virus-positive, one; malignancy, 10; and inflammatory diseases, two.

Six hundred ninety-five patients who were eligible for the urine analysis were tested following the protocol. Leukocytes and/or nitrite were positive in 25 patients, and protein was positive in 108 patients (Fig. 1). The prevalence of macroproteinuria was 16.2% (95% CI, 13.5–19.1%). MAU was tested in the remaining 562 patients. It was found to be positive in 171 patients. The prevalence of MAU was 25.5% (95% CI, 22.4–29%).

FIG. 1.

Patient population. SG, specific gravity.

The mean age of the analyzed study population (n = 670) was 52.13 ± 9.9 years. There were 387 men and 283 women. The mean BMI was 26.19 ± 4.34 kg/m². Of the subjects, 57.6% were obese. An alarming 16.3% had a BMI of >30 kg/m². The mean age at diagnosis of diabetes was 45.46 ± 9.81 years. The median duration of diabetes was 5 years. There were 146 patients with duration of diagnosed DM ≤1 year. Hypertension was self-reported in 42.5% and newly diagnosed in 16.1%. The mean fasting plasma glucose and HbA1C were 155.6 ± 56.4 mg/dL and 7.8 ± 1.6%, respectively.

The prevalence of documented coronary artery disease was 16%, and that of documented cerebrovascular disease was 2.8%. Formal fundus evaluation was done in 445 subjects, of which 15.7% had nonproliferative diabetic retinopathy and 10.7% had proliferative diabetic retinopathy. Among the 47 patients with chronic renal failure, retinopathy was documented in 22 patients.

Insulin was used for glycemic control in 18.2% of the patients. The BMI of those patients taking insulin (24.9 ± 4.0 kg/m²) was significantly lower than that of patients taking oral hypoglycemic drugs (26.5 ± 4.3 kg/m²). The most common antihypertensive drug prescribed as monotherapy was angiotensin converting enzyme inhibitors (10.6%), followed by calcium channel blockers (7.7%), angiotensin receptor blockers (6.6%), and β-blockers (4.9%). A two-drug combination for the control of hypertension was used in 29.4% of the hypertensive population.

Patients were divided into three groups: normoalbuminuric, microalbuminuric, and macroproteinuric, as defined already. Table 1 represents the clinical and biochemical characteristics of these three groups. The mean age was comparable in all three groups. Gender distribution was not significantly different between normoalbuminuric and microalbuminuric groups, but men outnumbered women in the macroproteinuric group. The number of current smokers was similar in the three groups. Duration of diabetes was significantly higher in the macroproteinuric subjects (10.3 years) when compared to the microalbuminuric (6.2 years) and normoalbuminuric (5.8 years) subjects.

Table 1.

Clinical and Biochemical Characteristics of the Study Population

Characteristic	Normoalbuminuric	Microalbuminuric	Macroproteinuric
n	391	171	108
Men/women	216/175	98/73	73/35
Age (years)	51.5 ± 10.5	52.4 ± 9.44	53.93 ± 8.84
Duration of DM (years)	5.8 ± 5.9	6.3 ± 5.6*	10.3 ± 6.9*
Hypertension
Self-reported	139 (35.5%)	78 (45.6%)	69 (63.9%)*
Newly diagnosed	66 (16.9%)	30 (17.5%)	12 (11.1%)
Current smoking	34 (8.6%)	21 (12.2%)	15 (13.9%)
BMI (kg/m²)	26.3 ± 4.2	26.9 ± 4.43	24.7 ± 4.36^†
Waist circumference (cm)	93.5 ± 9.1	95.0 ± 10.4	90.5 ± 10.5^†
Blood pressure (mm Hg)
Systolic	134.3 ± 17.87	139.45 ± 18.99^†	144.44 ± 19.42*
Diastolic	85.08 ± 9.64	87.98 ± 9.67^†	89.46 ± 10.08*
Retinopathy^a	34 (8.7%)	36 (21.1%)	48 (44.4%)
Documented
Coronary artery disease	14.6%	20.5%	13.9%
Cerebrovascular disease	2.6%	2.9%	3.7%
Fasting plasma glucose (mg/dL)	147 ± 51.34	160.7 ± 51.9^†	176.37 ± 72.8*
HbA1C (%)	7.63 ± 1.61	7.99 ± 1.4	8.36 ± 1.7
Serum creatinine (mg/dL)	0.96 ± 0.16	1.005 ± 0.19^†	1.15 ± 0.23*
Estimated glomerular filtration rate (mL/min/1.73 m²)	79.72 ± 17.61	77.32 ± 23.04	67.63 ± 18.8*
Insulin therapy	59 (15.1%)	24 (14%)	31 (28.7%)^†
Angiotensin converting enzyme inhibitor or angiotensin receptor blocker therapy	60 (15.3%)	43 (25.1%)	43 (39.8%)^†

Data are mean ± SD values or n (%).

Percentage represents the proportion among those who were formally evaluated by an ophthalmologist.

*P < 0.0001 versus normoalbuminuric; ^† P < 0.05 versus normoalbuminuric.

The mean BMI values of the normoalbuminuric and microalbuminuric groups were not different. Waist circumference was higher in the microalbuminuric group. However, the macroproteinuric group had significantly lower BMI and waist circumference than the other two groups (P < 0.05). Both self-reported and newly diagnosed hypertension conditions were more prevalent in the albuminuric groups compared to the normoalbuminuric subjects. The mean systolic and diastolic blood pressures were significantly higher in the microalbuminuric and macroproteinuric groups. Past documented coronary artery disease events were more common in the microalbuminuric group than the macroproteinuric group. This did not reach statistical significance. Similar trend was not observed with cerebrovascular disease events.

Fasting plasma glucose, HbA1C, and serum creatinine values were highest among the macroproteinuric group, followed by the microalbuminuric group. The estimated glomerular filtration rate decreased, and retinopathy increased progressively, from the normoalbuminuric to macroproteinuric group. Significantly more patients were taking insulin in the macroproteinuric group compared to the normoalbuminuric and microalbuminuric group (P < 0.0001). Among those with duration of diabetes ≤1 year, 24.7% had MAU, 6.2% had macroproteinuria, and 9.4% had documented retinopathy.

Risk factors

In univariate analysis, hypertension, presence of retinopathy, glycemic control, angiotensin receptor blocker intake, and calcium channel blocker intake were significantly associated with MAU. But after applying multiple regression analysis, only retinopathy, HbA1C (>8.0%), and calcium channel blocker therapy remained significant. Duration of diabetes, duration of hypertension, smoking, BMI, waist circumference, and insulin therapy were not significantly associated in the multivariate analysis.

For macroproteinuria, male gender, duration of diabetes, duration of hypertension, retinopathy, angiotensin receptor blocker and calcium channel blocker intake, and insulin therapy were significantly positively associated in univariate analysis. Waist circumference was negatively associated with macroproteinuria. After multiple regression analysis, retinopathy, waist circumference, glycemic control, and calcium channel blocker intake remained as the risk factors for predicting macroproteinuria. Table 2 presents the results of the multiple logistic regression analysis for MAU and macroproteinuria.

Table 2.

Multiple Logistic Regression Analysis

	Odds ratio (95% CI) for
Parameter	MAU	Macroproteinuria
Age (years)	1.15 (0.72–1.85)	1.27 (0.67–2.41)
Duration of known diabetes (vs. ≤5 years)	1.13 (0.07–1.96)	1.45 (0.67–3.15)
Presence of hypertension	0.99 (0.54–1.72)	1.74 (0.83–3.7)
Documented retinopathy	2.95 (1.61–5.41)*	4.62 (2.26–9.41)*
Smoking	1.46 (0.84–2.56)	1.06 (0.46–2.41)
BMI (>25 kg/m²)	1.06 (0.57–1.96)	0.93 (0.41–2.10)
Waist circumference	1.43 (0.83–2.47)	0.41 (0.22–0.57)^†
HbA1C (>8.0%)	2.15 (1.36–3.40)^†	2.59 (1.33–5.03)^†
Insulin therapy	0.90 (0.51–1.59)	1.41 (0.74–2.67)
Calcium channel blocker therapy	2.70 (1.53–4.76)^†	2.24 (1.05–4.78)^†

*P < 0.0001 versus normoalbuminuric; ^† P < 0.05 versus normoalbuminuric.

Discussion

Epidemiological studies in different populations, including migrant Asians, native Asians, and Indians, have reported marked variations in the prevalence of MAU. Studies from migrant Asians in Britain showed a prevalence of 14–26%.^11,12 A study in New Zealand showed a prevalence of 14% in migrant Asians.¹⁴ To date, the largest study conducted in the native Asian population is the MicroAlbuminuria Prevalence (MAP) Study,²⁹ which showed an alarming prevalence of 39.8%. This study did not include Indians.

John et al.¹⁸ from Vellore and Viswanathan et al.¹⁹ from Chennai reported MAU prevalences of 19.7% and 26.5%, respectively. Yajnik et al.³⁰ reported from Pune that 23% of non–insulin-dependent DM and 19% of impaired glucose tolerance patients had MAU. A large clinic-based study done by Varghese et al.²⁰ in Chennai reported the prevalence of MAU to be 36.6%. A community-based study, CURES 45,²¹ from Chennai had shown an MAU prevalence of 26.9%. In the present study, the prevalence of MAU and macroproteinuria are 25.5% and 16.2%, respectively. This prevalence of MAU is comparable to that of Viswanathan et al.,¹⁹ CURES 45,²¹ and Yajnik et al.³⁰ The larger MAP Study²⁹ showed a much higher prevalence of 39.8%. However, this study included hypertensive type 2 diabetes patients. In our study, if only the hypertensive diabetes subjects are analyzed, the prevalence of MAU increases to 35.6%.

Previous studies in newly diagnosed diabetes have reported 23% prevalence of MAU in Pune³⁰ and 23.8% in Chennai.²¹ In the same studies, macroproteinuria was detected in 1.4% and 5.3%, respectively, of subjects with newly diagnosed diabetes. In our study, the prevalence of MAU in patients with known diabetes <1 year was 24.7%, and that of macroproteinuria was 6.2%. The proportion of patients who had albuminuria within the first year of diagnosis of diabetes is substantial. Only 41.4% subjects had a target blood pressure of less than 130/85 mm Hg. Of the hypertensive patients, 36% were prescribed an angiotensin converting enzyme inhibitor or angiotensin receptor blocker, either alone or in combination with other drugs.

Various risk factors have been found to be associated with MAU in different studies. Older age, male gender, longer duration of diabetes, smoking, BMI, waist:hip ratio, blood pressure, fasting blood glucose, HbA1C, retinopathy, and insulin therapy have been shown to be important. In the present study we found preexisting retinopathy, HbA1C, and calcium channel blocker intake to be significantly associated with MAU. The association with calcium channel blockers may reflect the severity of hypertension rather than the drug's direct effect. This has been documented in larger studies like the MAP Study.²⁹ Apart from the above risk factors, decreased waist circumference and insulin therapy were additional risk factors for macroproteinuria.

Alhough there may not be a causal relationship, the negative association between waist circumference and macroproteinuria is noteworthy. It is interesting to note that even the landmark UKPDS reported a paradoxical association between waist circumference and renal outcomes. They observed that increased central obesity was linked to albuminuria and that decreased waist circumference was associated with renal impairment.¹⁶ The basis for this discordance in risk factors is not clearly understood. The UKPDS investigators speculated that this difference may reflect the finding that albuminuria and renal dysfunction in type 2 diabetes have different pathogenetic mechanisms.¹⁶ Distinct sets of risk factors for these two outcomes also support the newer concept that MAU and diabetic nephropathy are not inextricably linked, especially in type 2 diabetes.¹⁶

The strength of our study is its good sample size. Also, there are no similar studies from North India, which constitutes roughly 25%³¹ of the Indian population. There are certain limitations in our study. The strip used for MAU detection was semiquantitative. However, the American Diabetes Association³² acknowledges that this technique has acceptable sensitivity and specificity with the caution that any positivity to be reconfirmed by other specific methods. Also, in the MAP Study²⁹ the test strips were validated with immunochemical assay and found to have 91.9% sensitivity and 63.4% specificity. Compared to the immunoturbidimetric assay, the sensitivity and specificity were 95% and 80%, respectively.

The urine sample in our study was a single, spot random morning sample. Hence the results would have been influenced by day-to-day variability and the pH and concentration of the urine. However, because the present study is a cross-sectional prevalence study, MAU detection in a spot urine sample by strips may be considered adequate. Also, we excluded urine samples that tested abnormal for pH and specific gravity by Combur 10.

Approximately every fourth patient with diabetes had albuminuria within a year after diagnosis. This high proportion probably indicates a longer duration of prior undiagnosed diabetes. Distinct sets of risk factors exist for MAU and macroproteinuria in type 2 diabetes, supporting the notion that they may be pathophysiologically different. Although MAU is the best available noninvasive parameter to identify those at risk of developing diabetic nephropathy, additional new risk markers need to be investigated. Such risk markers will help us to focus preventive measures in those who are at reversible stages of complications, thus reducing the socioeconomic burden at both the individual and the national level.

Footnotes

Author Disclosure Statement

The authors declare that they have no conflict of interest.

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Prevalence of Microalbuminuria Among Patients with Type 2 Diabetes Mellitus—A Hospital-Based Study from North India

Abstract

Background:

Methods:

Results:

Conclusions:

Introduction

Subjects and Methods

Subjects

Methods

Definitions

Statistical analysis

Results

Risk factors

Discussion

Footnotes

Author Disclosure Statement

References