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NDT Advance Access published online on August 6, 2008
Nephrology Dialysis Transplantation, doi:10.1093/ndt/gfn447
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© The Author [2008]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org


Socioeconomic status and microalbuminuria in an Asian population

Charumathi Sabanayagam1, Anoop Shankar1, Seang Mei Saw1,2, Su Chi Lim3, E Shyong Tai4 and Yin Wong2,5

1 Department of Community, Occupational, and Family Medicine, Yong Loo Lin School of Medicine, National University of Singapore 2 Singapore National Eye Centre and Singapore Eye Research Institute 3 Alexandra Hospital 4 Singapore General Hospital, Singapore 5 Centre for Eye Research Australia, University of Melbourne, Melbourne, Australia

Correspondence and offprint requests to: Anoop Shankar, Department of Community Medicine, West Virginia University School of Medicine, P.O. Box 9190, Morgantown, WV 26506-9190. Tel: (304) 293-0199; Fax: (304) 293-6685; E-mail: ashankar{at}hsc.wvu.edu



   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Background. In studies from developed Western countries, lower socioeconomic status (SES) has been reported to be associated with kidney diseases. However, this hypothesis has not been examined in populations from newly industrialized Asian countries. We evaluated the association between SES and micro/macroalbuminuria in a population-based sample in Singapore.

Methods. We examined 920 participants of Malay ethnicity aged 40–80 years (49.6% female). SES was defined through education, income and housing type of participants. The main outcome of interest was the presence of micro/macroalbuminuria defined as a urinary albumin-to-creatinine ratio (ACR) ≥17 mg/g for men and ≥25 mg/g for women.

Results. Lower categories of SES were associated with micro/macroalbuminuria; compared to the higher categories of SES, the odds ratio (95% confidence interval) of micro/macroalbuminuria was 1.76 (1.23–2.52) for primary/lower education, 1.64 (1.16–2.31) for income <1000 Singapore dollars (SGD)/retired status, 1.44 (1.01–2.06) for small/medium housing type and 2.37 (1.56–3.60) for the coexistence of all three low SES factors (primary/ below education, income <1000 SGD/retired status and small/medium housing type) compared to ≤1 low SES factor. This pattern of association was consistently present in subgroup analyses by gender and age.

Conclusions. Lower SES is associated with the presence of micro/macroalbuminuria independent of age, gender, smoking, alcohol intake and body mass index among Malay adults in Singapore.

Keywords: education; housing type; income; kidney disease; microalbuminuria



   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Microalbuminuria is a marker of chronic kidney damage and a risk factor for the progression of kidney and cardiovascular diseases [1,2]. Studies have shown that microalbuminuria is predictive of diabetic nephropathy [3], hypertensive renal disease [4], and renal dysfunction in non-diabetic subjects [5] and in the general population [6].

In addition to established risk factors such as diabetes mellitus and hypertension [7], socioeconomic status (SES) is increasingly recognized as an important predictor for kidney disease, largely based on studies conducted among Western populations [8–10]. However, the association of SES with microalbuminuria has not been fully examined in other racial/ethnic groups and other countries, such as in Asian populations, where diabetes mellitus and hypertension are highly prevalent, but socioeconomic conditions are vastly different [11,12]. In this context, we examined the association between SES and micro/macroalbuminuria, a marker of kidney disease, in a population-based study in Singapore.



   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
The present analysis was based on data from the Singapore Malay Eye Study (SiMES), a population-based, cross-sectional study of Malay adults mainly aimed to collect information related to major eye conditions and the public health impact of the common age-related eye diseases affecting urban Malay people living in Asia. Detailed descriptions of the study population and methodology have been previously published [13]. In brief, an age-stratified random sample of the Malay population aged 40–80 years was drawn from the computer-generated random list of 16 069 Malay names provided by the Ministry of Home Affairs. Of the 5600 individuals selected, 4186 were found to be eligible to participate in the study. A total of 3280 individuals participated in the study (response rate = 78.7%) [13] of whom 944 provided urine samples for measuring albumin and creatinine. After excluding participants with missing data on SES and selected other factors, the final sample for analysis included 920 participants. Compared with those included in the final analysis, excluded participants were older, lesser educated, earning less and living in smaller houses (P < 0.05).

Outcome of interest
Spot untimed urine samples were collected for measurement of albumin and creatinine. Albumin was measured in mg/L and creatinine in mmol/L. The ratio of urine albumin-to-creatinine (ACR) concentration expressed in µg/mg was used to estimate total daily albumin excretion. Microalbuminuria was defined as a urinary ACR of 17–250 mg/g for men and 25–355 mg/g for women, and macroalbuminuria was defined as urinary ACR >250 mg/g for men and >355 mg/g for women based on the National Kidney Foundation's Kidney Disease Outcome Quality Initiative working group definition [7]. The main outcome of interest in the current study was the presence of micro/macroalbuminuria, defined as urine ACR levels >17 mg/g for men and >25 mg/g for women.

Measurement of exposure variables
Age was defined as the age at the time of examination and categorized into ranges of 40–44, 45–49, 50–54, 54–59, 60–64, 64–69, 70–74 and 75–81 years. Information on education, income, housing, life style factors and medical history was ascertained through questionnaire. Educational level was grouped into three categories based on the highest educational level attained by the participants: (1) primary (elementary) or lower (≤6 years), (2) secondary (high school) (7–10 years) and (3) post-secondary (≥11 years, including university education). Income level was defined as individual monthly income in Singapore dollars (SGD) and divided into three categories: (1) low (<SGD1000), (2) middle (SGD1000 to <2000) and (3) high (≥SGD2000). Housing type was classified as follows: (1) small (1- to 2-room public flat), (2) medium (3- to 4-room public flat) and (3) large (5-room public flat or private housing). Finally, to test for the potential additive effects of the SES factors, participants were grouped into categories based on the coexistence of lower categories of the three SES factors (primary/below education, income <1000 SGD/retired and housing type small/medium) into (1) having all three low SES factors, (2) having a combination of any two of the three low SES factors and (3) having ≤1 low SES factor. Smoking status was categorized into never smoker, former smoker and current smoker. Alcohol consumption was categorized into drinkers, if the participants ever consumed alcohol (irrespective of quantity), and non-drinkers. Body mass index (BMI) was calculated as weight in kilograms divided by the square of height in metres (kg/m2). Blood pressure (BP) was measured with a digital automatic blood pressure monitor after the participants were seated for at least 5 min. Hypertension was defined as systolic BP ≥140 mmHg or diastolic BP ≥90 mmHg or self-reported previously diagnosed hypertension. We calculated the mean arterial BP as 1/3 (systolic BP) + 2/3 (diastolic BP). Glycosylated haemoglobin (HbA1C) and casual blood glucose were measured from a venous sample collected from the participants. Diabetes mellitus was defined as a casual plasma glucose ≥200 mg/ dL (11.1 mmol/L) or self-reported physician-diagnosed diabetes or use of glucose-lowering medication.

Statistical analysis
We combined micro- and macroalbuminuria categories as the prevalence of macroalbuminuria was low (4.9%) in the study population. The prevalence of micro/macro- albuminuria was calculated stratified by SES and selected factors. Tests for linear trend across categories of education, income and housing were performed using the corresponding SES indicator as an ordinal variable in logistic regression models. We examined the association between each measure of SES and micro/macroalbuminuria in two multivariable models. In the first model, we adjusted for age (years), gender (female, male), smoking status (never, former, current), alcohol intake (no, yes) and BMI (kg/m2). In the second model, we additionally adjusted for diabetes mellitus (no, yes), hypertension (no, yes), HbA1C (%) and mean arterial BP (mm Hg). For these analyses, SES indicators were included as dichotomous variables using the highest SES category, namely, secondary and above edu- cation, income ≥SGD1000 and large/private housing as reference categories. We also tested the association of micro/macroalbuminuria with the coexistence of low SES factors using ≤1 low SES factor as the reference category. To explore the consistency of the observed association between SES and micro/macroalbuminuria, we performed stratified analyses by age group and gender. All statistical analyses were performed using SAS version 9.1.



   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
The mean age of the study participants was 56.2 years with 49.6% being women. Older individuals were less likely to have secondary/higher education, to earn higher income and to live in large/private housing. A majority of the men (75.4%) were either current or past smokers. 67.4% of the participants had hypertension (mean age, 60 years; 36.3% women) and 20% had diabetes mellitus (mean age, 58.9 years; 10.5% women). Those with diabetes had significantly higher BMI (27.1 kg/m2) compared to non-diabetics (26.0 kg/m2) P = 0.005. Further, we also assessed retinopathy changes among the study participants as the present study included eye changes. The prevalence and severity of retinopathy were defined according to modified Airlie House Classification [14]. The prevalence of retinopathy among those with diabetes was 35.3% (moderate to severe, 16.5%) and among those with hypertension was 15.7% (moderate to severe, 5.2%). Among the study participants, 12% reported having previous history of myocardial infarction or angina or stroke.

Table 1 presents the prevalence of micro/macro- albuminuria by SES and selected factors. The prevalence of micro/macroalbuminuria was 36.9% in the whole cohort. The prevalence increased with increasing categories of age (P-trend <0.0001). In contrast, the prevalence decreased with increasing categories of education and income (P-trend <0.05). Among the three housing types we examined, the majority (70%) of the study population lived in medium housing (3- to 4-room public apartments). The prevalence of micro/macroalbuminuria was highest among those living in smaller houses and lowest among those living in larger/private apartments (P < 0.05). Over half (56%) of the study population was overweight/obese with BMI ≥25 kg/m2. Overweight/obesity was significantly associated with micro/macroalbuminuria (P < 0.05). No significant difference was detected in the prevalence of micro/macroalbuminuria by gender or smoking status.


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  		Table 1 Prevalence of micro/macroalbuminuria by socioeconomic status (SES) and selected factors

 
Table 2 presents the odds ratios of micro/macro- albuminuria by SES categories. In multivariate analyses adjusted for age, gender, smoking status, alcohol intake and BMI primary/below education, income <1000 SGD/retired status and small/medium housing type were found to be positively associated with micro/macroalbuminuria. In this sample of Malay adults, 22.0% had ≤1 low SES factor, 31.0% had two low SES factors and 42.8% had all the three low SES factors studied. The prevalence of micro/macroalbuminuria increased stepwise with the increase in the number of SES factors (P-trend <0.0005) and the coexistence of all three low SES factors showed a significant positive association with micro/macroalbuminuria compared to ≤1 low SES factor. In the multivariable model 2, where we additionally adjusted for diabetes, hypertension, HbA1C and mean arterial BP, the overall positive association between SES and micro/macroalbuminuria persisted; however, the ORs were attenuated for most associations.


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  		Table 2 Association between socioeconomic status (SES) and micro/macroalbuminuria

 
In subgroup analysis stratified by gender (Table 3), and by age group (Table 4), the inverse association between education, income, housing type and low SES factors was also consistently present within these subgroups, and multivariable OR estimates ranged from 1.17 to 3.08 within gender and 1.09 to 2.49 within age subgroups for model 1 and ranged from 1.06 to 2.05 within gender and 1.20 to 2.67 within age subgroups for model 2.


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  		Table 3 Association between socioeconomic status (SES) and micro/macroalbuminuria by gender

 

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  		Table 4 Association between socioeconomic status (SES) and micro/macroalbuminuria by the age group

 
In another supplementary analysis, we evaluated the association of SES with diabetes mellitus and hypertension, potential mediating factors of kidney disease. The prevalence of both diabetes mellitus and hypertension was higher among those with primary/below education, income <1000 SGD/retired and living in small/medium housing type compared to those with secondary and above education, income ≥SGD1000 and large/private housing. Compared to those with ≤1 low SES factor, the multivariable OR (95% CI) among those with all three low SES factors was 2.96 (1.75–5.02) for diabetes mellitus and 1.71 (1.13–2.58) for hypertension.



   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
In a population-based study of Asian Malay adults, lower SES, as measured by education, income and housing type, was associated with micro/macroalbuminuria, independent of age, gender, smoking, alcohol intake and BMI. This inverse association between SES and micro/ macroalbuminuria persisted in subgroup analyses by gender and age group. Further, the coexistence of the lower categories of all three SES factors, namely primary/below education, income <1000 SGD/retired status and living in small/medium housing type was significantly associated with micro/macroalbuminuria compared to those with ≤1 low SES factor. These findings suggest that SES may be a risk marker and mediate processes associated with the development of kidney disease.

The urinary ACR ratio is a sensitive indicator of glomerular disease [7]. Micro/macroalbuminuria, an established and the most frequently studied marker of kidney damage in clinical [2] and epidemiological studies [15], has been identified as a risk factor for renal [6] and cardiovascular morbidity and mortality [2]. Microalbuminuria is predictive of poor renal function in diabetic subjects [3], non-diabetic subjects [5], hypertensives [4] and in the general population [6]. Persistent micro/macroalbuminuria (two of three measurements greater than the reference range) with glomerular filtration rate (GFR) ≥60 mL/min/1.73 m2 represents stages 1 and 2 of chronic kidney disease [7]. In NHANES III, the overall prevalence of micro/macroalbuminuria in adults aged 20 and above was 11.7% based on a single spot urine test [7,15]. The higher prevalence of micro/ macroalbuminuria (36.9%) observed in our study population could be attributed to the older age and the increased prevalence of diabetes and hypertension of the study population. In the current study, smoking and gender were not found to be associated with micro/macroalbuminuria. It is possible that smokers in our study may have changed their life style after being diagnosed with diabetes or hypertension. Also, our assessment of smoking status was rather crude and the lack of information on duration and pack-years of smoking may have introduced a bias reducing our ability to detect a true association. The exact reason why we did not observe an association between gender and micro/macroalbuminuria in our study is not clear. While several studies have reported a positive association between micro/macroalbuminuria and male gender [10,16], some studies have reported no association [17]. It is also possible that any putative association between male gender and micro/macroalbuminuria is not as pronounced among Asians compared to Western populations, due to differences in built and body surface area [18–20]. We believe that future studies with larger sample sizes and longer follow-up data are required before concluding on the nature of the association between gender and micro/macroalbuminuria.

Our finding of an inverse association between SES and micro/macroalbuminuria is in accordance with previous cross-sectional [10], and longitudinal studies [8,9] in Western populations that evaluated the association between SES and kidney damage. In our analyses, the pattern of association observed was very similar for all three measures of SES assessed. Education, the most widely used measure of SES in epidemiological studies, imparts health-related knowledge, promotes positive health behaviours and reflects access to resources during the early part of a person's life [21]. Income, an indicator of material resources, provides access to high-quality education, better housing and access to preventive healthcare services [22]. Housing reflects economic and social status of an individual and his or her family and operates through other SES indicators such as income, education and occupation [23].

Several studies have reported an inverse association between SES and various markers of kidney disease including elevated serum creatinine [8], decreased GFR [9] and albuminuria [10] similar to our findings. In the biracial Atherosclerosis Risk in Communities Study (ARIC) involving men and women aged 45–64 years, Merkin et al. [8] reported a greater risk of chronic kidney disease among white men living in low SES areas, the association was not significant among white women and African American men and women. In the Cardiovascular Health Study, residing in a low SES area was associated with kidney disease in an elderly US population [24]. Shoham et al. [9] reported that individual working class and life-course SES were associated with kidney disease. In the Third National Health and Nutrition Examination Survey (NHANES), Martin et al. [10] reported a positive association between poverty and kidney disease. Similar associations of lower SES with end-stage renal disease [25] and cardiovascular diseases [26] have been reported by several studies conducted in the USA and other developed countries. As micro/macroalbuminuria is an independent predictor of coronary artery disease and mortality [27], a corollary observation to our findings is that the reported inverse association between SES and increased risk of all-cause and coronary disease mortality [26] may be partially mediated through kidney damage.

Several mechanisms have been postulated to explain the relation between SES and micro/macroalbuminuria. It is plausible that SES may affect kidney function through more proximal risk factors of kidney disease such as diabetes mellitus and hypertension. In our study, the higher prevalence of diabetes mellitus and hypertension among low SES participants and the attenuation of the association between SES and micro/macroalbuminuria in multivariable model 2 that additionally adjusted for diabetes, hypertension, HbA1C and mean arterial BP suggest that at least part of the observed association between SES and micro/macroalbuminuria is mediated through hypertension and diabetes mellitus. Several studies from developed Western countries have reported similar inverse associations between SES and hypertension, and diabetes mellitus [26]. Other possible explanations for the observed inverse association between SES and micro/macroalbuminuria include the limited access of low SES subjects to healthcare services [25], increased occupational exposure to nephrotoxins such as heavy metals, solvents, etc. among occupations representing low SES status [28]. Low birth weight, which is a frequent finding associated with low SES [29], has been shown to be associated with the development of kidney disease in later life [7].

The main strengths of our study include its population-based sample, inclusion of ethnically homogeneous Malay population thus eliminating confounding by race ethnicity and the use of individual measures of SES factors. Our findings are also applicable to other ethnic Malay population in urban areas of Southeast Asia. Finally, we believe that this is the first study from a newly industrialized Asian country on the association between SES and kidney disease. Limitations of our study include possible bias resulting from exclusion of some eligible participants from the present analysis due to missing data on the urinary ACR. If our results are true, such a bias would result in underestimation of the true association, since those who were excluded from the analysis belonged to the lower SES categories compared to those who were included in the analysis. Secondly, the use of casual plasma glucose instead of fasting plasma glucose could have resulted in misclassification of diabetes status. Thirdly, we did not have information on medication use such as angiotensin-converting enzyme (ACE) inhibitors, or angiotensin II receptor blockers (ARB) that might have reversed or regressed the albuminuria status [30]. Finally, the cross-sectional nature of the study limits making causal inferences as regards the association between SES and micro/macroalbuminuria.

In conclusion, results from this population-based sample of Asian Malay adults in Singapore suggest that lower SES defined by education, income and housing type was inversely associated with micro/macroalbuminuria, independent of age, gender, smoking, alcohol intake and BMI. Our findings provide further evidence of the importance of SES factors as risk markers of chronic diseases, and may have important public health implications in targeting the low SES group in screening and prevention programmes for chronic kidney disease and its risk factors such as diabetes mellitus and hypertension.



   Acknowledgments
 
This study was supported and funded by the National Medical Research Council (NMRC), 0796/2003 & the Biomedical Research Council (BMRC), 078-305, 501/1/25-5, with support from the Singapore Prospective Study Program and the Singapore Tissue Network, A*STAR. The authors thank the staff and participants in the SiMES study for their important contributions.

Conflict of interest statement. None declared.



   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Received for publication: 9. 1.08
Accepted in revised form: 11. 7.08


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