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18]

Saudi J Kidney Dis Transpl 2016;27(2):348-355

2016 Saudi Center for Organ Transplantation Saudi Journal
of Kidney Diseases
and Transplantation

Renal Data from the Arab World

Prevalence and Determinants of Microalbuminurea Among Type 2

Diabetes Mellitus Patients, Baghdad, Iraq, 2013
Ali Abdalkader Ali1, Faris Hassan Al Lami2
1
NCD Department, Directorate of Public Health, Ministry of Health, 2Community and Family
Medicine Department, College of Medicine, Baghdad University, Baghdad, Iraq

ABSTRACT. Microalbuminuria (MAU) is an early marker of diabetic nephropathy (DN), which

accounts for a significant reduction in life expectancy of diabetic patients. The progression of DN
from the appearance of clinical proteinuria to end stage renal failure is usually irreversible.
Increased levels of urinary albumin secretion may represent a more generalized vascular damage.
This is the first study conducted in Iraq to determine the prevalence and potential risk factors of
MAU among Type 2 diabetes mellitus (T2DM) patients. A cross-sectional study was conducted
on a systematic random sample of 224 eligible T2DM patients aged 2564 years attending a DM
clinic in Baghdad. A questionnaire was developed to gather basic and clinical data, besides
anthropometric measurements, and laboratory assessment of lipid profile, HbA1c, serum crea-
tinine, albumin, and microalbumin/creatinin in urine. MAU was defined as albumin/creatinine ratio
30300 mg/g on two occasions. Only 36 cases (16.1%) had MAU. A statistical significant asso-
ciation found between MAU and educational level (P = 0.009), family history of hypertension (P
= 0.024) and DN (P = 0.013), history of hypertension (P = 0.001), duration of angiotensin-
converting-enzyme inhibitor drug intake in hypertensive patients (P = 0.001), body mass index
(BMI) (P = 0.014), and waist to hip ratio (P = 0.006). Logistic regression analyses revealed two
independent risk factors influencing MAU: diastolic blood pressure [odds ratio (OR) = 1.08, 95%
confidence interval (CI): 1.0071.118] and BMI (OR = 1.17, 95% CI: 1.0371.220). The preva-
lence of MAU is not low among DM patients. Mandatory screening of all DM patients and
amelioration of the assigned significant risk factors are recommended.

Introduction mellitus (T2DM) worldwide is reaching epide-

The increasing prevalence of Type 2 diabetes
Correspondence to:
Dr. Ali Abdalkader Ali,
NCD Department, Directorate of Public
Health, Ministry of Health, Baghdad, Iraq.
E-mail: alialazawi1967@yahoo.com
mic proportions and is becoming a major
public health problem.1 The importance of
T2DM is further emphasized by epidemiolo-
gical studies that clearly shows excess morta-
lity associated with T2DM, as well as an
increased risk of other T2DM-related compli-
cations which have a significant economic
impact on the health system worldwide.2
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Microalbuminurea in type 2 DM patients in Iraq
Around 1020% of people with T2DM die of
kidney failure.3,4 Diabetic nephropathy (DN)
accounts for a significant reduction in life
expectancy of diabetic patients. Microalbumi-
nuria (MAU) is an early marker of DN.5
Without any intervention, in T2DM patients,
2040% with MAU progress to overt nephro-
pathy and 20 years later, approximately 20%
develop end stage renal disease (ESRD).6
MAU in diabetic patients is a risk factor for
cardiovascular disease, and identifies patients
who need more rigorous cardiovascular risk
management, especially more intensive blood
pressure control, and strict attention to glyce-
mic control and lipid levels.7-9 Recent studies
have demonstrated that the onset and course of
DN can be ameliorated to a very significant
degree by several interventions, but these
interventions have their greatest impact if
instituted at a point very early in the course of
the development of this complication. Thus,
the finding of MAU is an indication of scree-
ning for possible vascular disease and aggres-
sive intervention to reduce all cardiovascular
risk factors [e.g., lowering of low density lipo-
protein (LDL) cholesterol, antihypertensive
therapy, cessation of smoking, institution of
exercise, etc.].10 The progression of DN from
the appearance of clinical proteinuria to ESRD
is usually irreversible.6,11 Therefore, detection
of MAU as early as possible in the course of
the disease is very important.12
In Iraq, the prevalence of DM among adults
is 10.4%, which means that around three
million Iraqi individuals are suffering from
DM.13 In spite of this large number of DM
cases and the feasibility of prevention or de-
laying ESRD, little is known about the pro-
blem of early DN in the country. This study
was conducted to estimate the prevalence and
identify potential determinants of MAU among
T2DM patients attending a Diabetes Center in
Baghdad, Iraq, 2013.
Patients and Methods
A cross-sectional study conducted on a
systematic random sample of T2DM patients
attending the Diabetic Center in Eastern side
349
of Baghdad during the period January to May,
2013. The following variables were obtained
using a questionnaire filled through direct
interview with the study participants: age, sex,
level of education, marital status, smoking
habit, family history of hypertension and DM,
comorbid illnesses, and type of diabetes the-
rapy. Anthropometric measures (body mass
index (BMI) and waist to hip ratio) and blood
pressure were measured. Laboratory investi-
gations included lipid profile, HbA1c, serum
creatinine and albumin, and microalbumin/crea-
tinin in urine. Microalbuminurea was mea-
sured three times one month apart using early
morning urine specimen. Exclusion criteria
were the presence of overt proteinuria, urinary
tract infection, hematuria, ketonuria, pregnancy,
heart failure, and use of systemic steroids in
the past four weeks.
MAU is considered positive when urinary
albumin to creatinin ratio (ACR) is 30300
mg/g creatinin in two of the three tests within
36 months period in a spot urine sample.14,15
Measurement of urine creatinin was performed
by using (Reflotron Creatinine) test strip
utilizing Reflotron Plus Roche Germany and
measurement of urine micro-albumin was per-
formed by using ORG 5MA Micro-Albumin
Germany ELISA Kit utilizing Awareness
Technology, Inc., Micro plate Reader (USA).
Statistical analysis
The Statistical Package for Social Sciences
(SPSS) version 18 (SPSS Inc., Chicago, IL,
USA) used for data entry and analysis. Chi-
square test of independence was used to test
the association between categorical data. P
0.05 was considered significant. Logistic
regression analysis was performed to identify
the significant unconfounded risk factors.
Odds ratio (OR) and its 95% confidence
interval (CI) were calculated.
Official approval and ethical consideration
Approval of the Iraqi Ministry of Health was
granted and a written informed consent from
each participant was obtained.
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350 Ali AA, Al Lami FH

Results family history of DN (P = 0.013), hyper-

tension (P = 0.001), and the duration of angio-
The total number of eligible T2DM patients tensisn converting enzyme inhibitors (ACEIs)
who accepted to participate was 245; 224 pa- or angiotensin receptors blockers (ARBs)
tients continued in the study for the three visits. medication use (P = 0.001) (Table 2).
The overall response rate was 91.4%. The None of the DM-related characteristics pre-
number of the T2DM patients who tested sented in Table 3 showed a significant asso-
positive for MAU (ACR of 30300 mg/g on ciation with presence of MAU (P >0.05).
two occasions) was 36 making a prevalence Similarly, none of the following biochemical
rate of 16.1% (95% CI: 11.320.9%). attributes were significantly associated with
The age range was 2564 years; around 39% MAU: serum cholesterol (P = 0.08), serum tri-
of the patients were in the age category of 50 glyceride (TG) (P = 0.72), high-density lipo-
59 years; the least was in the age group 60+ protein (HDL)-cholesterol (P = 0.34), serum
years (8.9%). Male:female ratio was 1.4:1. LDL-cholesterol (P = 0.55), high serum crea-
A comparison of those with and without tinine (P = 0.59), and abnormal estimated glo-
MAU for sociodemographic variables re- merular filtration rate (eGFR) (P = 0.25)
vealed a significant association with marital (Table 4).
status (P = 0.001) and education status (P = The prevalence of MAU in the subjects with
0.009) (Table 1). normal BMI was 10%; compared to 9% and
A similar comparison was made for family 23% for overweight and obese subjects, res-
history for certain diseases, history of hyper- pectively, as shown in Table 5. A significant
tension and hypertension medication. A signi- association found between BMI and MAU (P
ficant association was found with positive = 0.014). The proportion of MAU was signi-
family history of hypertension (P = 0.024), ficantly higher in patients with central obesity
Table 1. Distribution of the study group by microalbuminurea and basic demographic characteristics,
smoking habit, and physical activity.
Microalbuminurea (ACR 30 and
300 mg/g on two occasions) Total
Demographic characteristic P
Negative Positive
n = 188 % n = 36 % n = 224 %
Age groups (years) 0.14
<40 25 71.0 10 29.0 35 15.6
4049 71 88.0 10 12.0 81 36.2
5059 76 86.0 12 14.0 88 39.3
60+ 16 80.0 4 20.0 20 8.9
Gender 0.77
Female 78 85.0 14 15.0 92 41.1
Male 110 83.0 22 17.0 132 58.9
Educational level 0.009
Illiterate/primary 64 74.4 22 25.6 86 38.4
Secondary 77 93.0 6 7.0 83 37.1
College/higher 47 86.0 8 14.0 55 24.5
Marital status 0.001
Single 6 50.0 6 50.0 12 5.4
Ever married 182 86.0 30 14.0 212 94.6
Smoking 0.20
Never smoke 120 83.0 25 17.0 145 64.7
Ex-smoker 24 77.0 7 23.0 31 13.8
Current smoker 44 92.0 4 8.0 48 21.5
ACR: Albumin to creatinin ratio.
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Microalbuminurea in type 2 DM patients in Iraq 351

Table 2. Distribution of the study group by microalbuminurea and family history for certain diseases,
comorbid illnesses and hypertension medication.
Microalbuminurea (ACR 30 and 300 mg/g on 2 occasions)
Negative Positive Total
P
n = 188 % n = 36 % n = 224 %
Positive family history in first
degree relatives
Hypertension 0.024
No 96 90.0 11 10.0 107 47.8
Yes 92 79.0 25 21.0 117 52.2
Diabetes mellitus 0.25
No 55 80.0 14 20.0 69 30.8
Yes 133 86.0 22 14.0 155 69.2
Diabetic nephropathy 0.013*
No 180 86.0 30 14.0 210 93.7
Yes 8 57.0 6 43.0 14 6.3
Comorbid illness
Hypertension 0.001
Negative 127 90.1 14 9.9 141 63.0
Positive 61 73.5 22 26.5 83 37.0
Hypertension duration (years) 0.89
1 25 75.8 8 24.2 33 14.7
1.16 22 73.3 8 26.7 30 13.4
6 14 70.0 6 30.0 20 8.9
Hypertension medication
ACEI or ARB users 0.15
No 28 66.7 14 33.3 42 18.7
Yes 33 80.5 8 19.5 41 18.3
ACEI or ARB intake duration (years) 0.001*
2 11 57.9 8 42.1 19 8.5
2+ 22 100.0 0 0.0 22 9.8
*Fishers exact test. ACR: Albumin to creatinin ratio, ACEI: Angiotensisn converting enzyme inhibitor,
ARB: Angiotensin receptors blocker.

(abnormal waist-hip ratio) compared to those
with normal waist-hip ratio (18%) (P = 0.006).
Logistic regression analysis was applied. MAU
was the dependant variable, and the following
were significant covariates: hypertension with
OR = 1.061, 95% CI: 1.0071.118, P = 0.026
and BMI with OR = 1.125, 95% CI: 1.037
1.220, P = 0.004.
Discussion
The prevalence of MAU in T2DM patients
was 16.1%. Several epidemiological studies
conducted in different Asian countries re-
ported prevalence rates of MAU ranging
between 8% and 32% among T2DM patients.16,17
The prevalence rate was similar to the result in
Saudi Arabia (16.8%),18 Iran (14.2%),19 and
Sweden (16%).20 However, the prevalence rate
was 27% in Oman,21 and 61% in the United
Arab Emirates.22 The difference may be attri-
buted to the differences in the age distribution
of the studied sample, the definition of MAU
and method of assessment.
The high prevalence among single patients
noticed in this study is consistent with a study
conducted in Iran, 2012 on 1557 patients aged
more than 18 years.23 This is supported by a
qualitative study that explored how spousal
support influences dietary changes following a
diagnosis of T2DM in middle-aged and older
adults.24
The significant association of MAU with
education status is consistent with a two years
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352 Ali AA, Al Lami FH

Table 3. Distribution of the study group by microalbuminurea and diabetes mellitus-related characteristics.
Microalbuminurea (ACR 30 and 300 mg/g on 2 occasions)
Negative Positive Total
P
n = 188 % n = 36 % n = 224 %
Duration of diabetes (years) 0.29
3 60 85.7 10 14.3 70 31.3
3.019.00 88 86.3 14 13.7 102 45.5
9.00 40 76.9 12 23.1 52 23.2
DM medication 0.06
No medication 11 100.0 0 0.0 11 4.9
Oral hypoglycemic agent 131 81.0 30 19.0 161 71.9
Insulin 35 95.0 2 5.0 37 16.5
Combined 11 73.0 4 27.0 15 6.7
Self-blood glucose monitoring 0.17
No 86 80.0 21 20.0 107 47.8
Yes 102 87.0 15 13.0 117 52.2
DM control (HbA1c%) 0.97
Controlled (<7) 31 84.0 6 16.0 37 16.5
Not controlled (7) 157 84.0 30 16.0 187 83.5
ACR: Albumin to creatinin ratio.

follow-up study conducted on 173 diabetic pa- vices relevant for diabetes care, and a worse
tients in The Netherlands. The study showed outcome in terms of complications.25 Similar
that diabetic people with low level of education findings were reported in a Chinese study in
have lower utilization rates of checks and ser- 2008.26
Table 4. Distribution of the study group by microalbuminurea and abnormal biochemical findings.
Microalbuminurea (ACR 30 and 300 mg/g on 2 occasions)
Negative Positive Total
P
n = 188 % n = 36 % n = 224 %
High serum cholesterol (200 mg/dL) 0.08
Positive 85 79.4 22 20.6 107 47.8
Negative 103 88.0 14 12.0 117 52.2
High serum TG (150 mg/dL) 0.72
Positive 136 84.5 25 15.5 161 71.9
Negative 52 82.5 11 17.5 63 28.1
Abnormally low serum HDL
0.34
(40 male and 50 mg/dL female)
Positive 130 85.5 22 14.5 152 67.9
Negative 58 80.6 14 19.4 72 32.1
High serum LDL ( 160 mg/dL) 0.55*
Positive 23 85.2 4 14.8 27 12.0
Negative 165 83.8 32 16.2 197 88.0
High serum creatinine
0.59*
(>1.4 male and >1.2 female mg/dL)
Abnormal 3 100.0 0 0.0 3 1.3
Normal 185 83.7 36 16.3 221 98.7
Abnormal eGFR (mL/min./1.73 m) 0.25
Abnormal 60 80.0 15 20.0 75 33.5
Normal 128 85.9 21 14.1 149 66.5
*Fishers exact test. ACR: Albumin to creatinin ratio, HDL: High-density lipoprotein, LDL: Low-density
lipoprotein, eGFR: Estimated glomerular filtration rate, TG: Triglyceride.
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Microalbuminurea in type 2 DM patients in Iraq 353

Table 5. Distribution of the study group by microalbuminurea and certain anthropometric measurements.
Microalbuminurea (ACR 30 and 300 mg/g on 2 occasions)
Negative Positive Total
P
n = 188 % n = 36 % n = 224 %
Body mass index (kg/m2) 0.014
Normal (<25) 28 90.0 3 10.0 31 13.8
Overweight (2529.9) 74 91.0 7 9.0 81 36.2
Obese (30+) 86 77.0 26 23.0 112 50.0
High waist hip ratio
0.006*
(male >0.9, female >0.85)
Normal 29 100.0 0 0.0 29 12.9
Abnormal 159 82.0 36 18.0 195 87.1
*Fishers exact test. ACR: Albumin to creatinin ratio.

The significant association of MAU with posi-
tive family history of hypertension is consis-
tent with a study conducted by Keller et al,
1996, in Germany.27 Similarly, the significant
association with positive family history of DN
is consistent with other studies that demons-
trated a genetic susceptibility contributing to
the development of DN in patients with both
T1DM and T2DM.28,29
Significant association was found between
hypertension and MAU which is consistent
with Al-Futaisi et al21 and Unnikrishnan et al30
studies. High diastolic blood pressure was a
significant independent risk factor for MAU
(OR = 1.061, 95% CI: 1.0071.118, P = 0.026).
This is consistent with other studies tackling
this variable.18,19
Regarding the use of ACEI or ARB medi-
cation among hypertensive patients, the preva-
lence of MAU showed no statistical signifi-
cance association with the use of ACEI or
ARB medication (P = 0.15). By further strati-
fication of the users by the duration of use (2
years and 2 years), a statistically significant
inverse association was seen with MAU by
binary analysis. Other studies also demons-
trated the inverse association with angiotensin-
converting-enzyme use.31,32 Similarly, obesity
(BMI 30) was also a significant risk factor in
binary and logistic regression analysis. This is
supported by two studies.22,30 The significant
association between MAU and waist hip ratio
is consistant with other studies conducted in
The Netherlands33 and China.34 The logistic
regression analysis did not prove this variable
as a significant factor.
In this study, no significant association was
found with age and sex. This is consistant with
many studies tackling these variables.17,19,35
Similarly, the following biochemical measures
were evaluated and were found not significantly
associated with MAU: HbA1c, serum choles-
terol, HDL, LDL, TG, and creatinin levels.
Many studies conducted in many countries
found similar results.18,19,35 The nonsignificant
association with eGFR is consistant with a
study conducted by Nosadini et al 2000 in
Italy.36
Conclusion
Around one of every six patients with T2DM
had MAU. High blood pressure and obesity
were significant predictors and should be cor-
rected. All T2DM patients should have regular
screening for MAU, and the health facilities
need to provide the necessary equipment to
conduct this investigation.
Since the study design is a cross-sectional,
temporal relationship cannot be ascertained.
Moreover, referral bias should be considered,
as the study conducted in a specialized center,
and the sample may not represent all patients
in the community.
Conflict of interest: None declared.
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