Diabetes & Metabolic Syndrome: Clinical Research & Reviews 12 (2018) 365–368

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Diabetes & Metabolic Syndrome: Clinical Research &

Reviews
journal homepage: www.elsevier.com/locate/dsx

Original Article

Intercellular adhesion molecule-1 in diabetic patients with and

without microalbuminuria
Zahra Karimia,b , Farima Kahea,b , Adeel Jamilc , Jolanta Marszalekd, Asiye Ghanbarib ,
Mohsen Afaridehb , Elias Khajehb , Sina Noshadb , Alireza Esteghamatib , Gerald Chia,*
a
Division of Cardiovascular Medicine, Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States
b
Endocrinology and Metabolism Research Center, Vali-Asr Hospital, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
c
James J. Peters Veterans Affairs Medical Center, Icahn School of Medicine at Mount Sinai, Bronx, New York, United States
d
Department of Neurology, University of Arkansas for Medical Sciences, Little Rock, AR, United States

A R T I C L E I N F O A B S T R A C T

Background: Nephropathy is a major complication of type 2 diabetes mellitus (T2DM) and is heralded by
Keywords: the insidious development of microalbuminuria (MA). It is suggested that the serum levels of
ICAM-1
Intercellular Adhesion Molecule-1 (ICAM-1) is correlated with diabetic nephropathy. In this cross-
Microalbuminuria
Diabetes mellitus
sectional study, we evaluated serum ICAM-1 level in diabetic patients with and without MA.
Methods: A total of 187 participants were enrolled and were classified into three groups including 40
healthy controls and 2 diabetic groups with (n = 59) or without MA (n = 88). Serum levels of ICAM-1,
fasting plasma glucose (FPG), hemoglobin A1c (HbA1c), total cholesterol, high density lipoprotein
cholesterol, low density lipoprotein cholesterol, very low density lipoprotein cholesterol and C-reactive
protein (CRP) were measured in all three groups. Statistical analyses were performed using the SPSS
software. A P-value less than 0.05 was considered statistically significant.
Results: Serum levels of ICAM-1 were significantly higher in diabetic patients irrespective of MA.
Moreover, ICAM-1 levels in patients with MA were significantly higher than patients without MA.
Patients with MA had significantly higher age and blood pressure compared to those without MA
(P = 0.001). Serum levels of ICAM-1 were significantly correlated with age and HbA1c.
Conclusions: Overall, serum ICAM-1 levels were significantly higher in T2DM patients with MA and it may
be associated with the severity of diabetic kidney disease.
© 2017 Diabetes India. Published by Elsevier Ltd. All rights reserved.

1. Introduction (ICAM-1) and other vascular adhesion molecules in patients with

In patient with type 2 diabetes mellitus (T2DM), nephropathy is
a progressive disorder of the microvasculature of the kidney which
may result in end-stage renal disease (ESRD) [1]. Microalbumi-
nuria (MA), defined as excretion of 30–300 mg of albumin in the
urine per 24 h (or 20–200 mg/min or 30–300 mg/mg creatinine),
marks the initial presentation in the spectrum of diabetic
nephropathy [2]. Numerous studies have reported increased
serum concentrations of intercellular adhesion molecule-1
Abbreviations: CRP, C-reactive protein; FPG, fasting plasma glucose; HbA1c,
hemoglobin A1c; ICAM-1, intercellular adhesion molecule-1; MA, microalbumi-
nuria; T2DM, type 2 diabetes mellitus.
* Corresponding author at: Division of Cardiovascular Medicine, Department of
Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, 330
Brookline Avenue, Suite OV-540, Boston, MA 02215 United States.
E-mail address: gerald.chi@baiminstitute.org (G. Chi).
T2DM [3–6]. The ICAM1 gene is located on chromosome 19p13 and
is a 90-KD cell surface glycoprotein [7,8]. Several factors induce
ICAM expression such as cytokines, reactive oxygen species (ROS)
and stress [9,10]. In general, expression of ICAM on the surface of
arterial endothelial cells is low, however several studies on diabetic
(both type 1 and 2) animals with nephropathy indicated
significantly increased levels of ICAM mRNA and protein expres-
sion [11–15]. Additionally, several lines of evidence have proven
higher levels of serum ICAM-1 in patients with type 1 diabetes in
comparison with normal population [16]. Therefore, it has been
proposed that ICAM-1 is an important factor for the development
of diabetes and diabetic nephropathy. ICAM-1 induces the
proliferation of T lymphocytes and facilitates the migration of
leukocytes to inflammation sites; in addition it triggers the release
of cytokines [17]. Moreover, clinical studies indicated that serum
ICAM-1 values increase in diabetic patients [18–20]. To the best of

https://doi.org/10.1016/j.dsx.2017.12.028
1871-4021/© 2017 Diabetes India. Published by Elsevier Ltd. All rights reserved.

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our knowledge, studies evaluating serum levels of ICAM in diabetic Table 1

Comparison of Clinical and biochemical characteristics.
patients in Iran are scarce; therefore, the study aims to perform
this cross-sectional study to evaluate ICAM-1 serum levels in the Control (n = 40) MA (n = 59) NMA (88) P-value
Iranian diabetic population with or without MA. Age 49.65  8.55 55.93  9.19 50.28  8.50 0.001
Sex Female 29 (29.6%) 21 (21.4%) 48 (49.0%) 0.001*
2. Methods Male 11 (12.4%) 38 (42.7%) 40 (44.9%)
ICAM-1 245.42  43.05 531.18  185.84 311.82  53.82 0.001
SBP 114.35  13.24 133.47  18.98 119.31  10.00 0.001
In the present study, 187 participants were enrolled and DBP 76.00  6.71 82.47  9.02 78.12  5.48 0.001
categorized to three groups including 40 healthy controls and two FBS 91.85  8.61 172.15  65.64 190.62  69.34 0.001
diabetic groups with or without MA (59 patients with MA and 88 HbA1c 4.99  0.41 8.24  1.39 8.28  1.59 0.001
patients without MA). Two diabetic groups were among patients Cholesterol 170.52  36.98 191.15  112.03 207.40  41.40 0.024
HDL 51.40  14.09 45.28  13.01 48.40  12.12 0.066
referred to the diabetes clinic of Vali-Asr Hospital. Type 2 diabetes
LDL 106.82  20.50 101.80  38.59 119.27  29.87 0.003
was diagnosed according to the American Diabetes Association CRP 1.01  0.38 1.77  1.11 2.48  1.89 0.001
diagnostic criteria [21], and MA was defined as more than 30 mg BMI 26.81  3.39 29.13  3.86 29.52  3.73 0.001
albumin in urine per day [2]. Patients with severe systemic Abbreviations: ICAM-1: intercellular adhesion molecule, SBP: systolic blood
diseases were excluded. Enrolled patients were fully examined; pressure; DBP: diastolic blood pressure; FBS: fasting blood sugar; HbA1c:
height and weight were measured and body mass index (BMI) was glycosylated hemoglobin; HDL: high-density lipoprotein; LDL: low-density
calculated (kg/m2). After an overnight 12 h of fasting, 10 ml of lipoprotein cholesterol; CRP: C-reactive protein: BMI: body mass index.

venous blood sample was collected from each participant and

serum levels of fasting plasma glucose (FPG) were determined
using the Glucose Oxidase Method. High-performance liquid
chromatography (HPLC) was performed to assess glycated without MA (P = 0.001). On the other hand, the mean level of FPG
hemoglobin (HbA1c). Serum concentrations of lipids, including (P = 0.10), HbA1c (P = 0.86), cholesterol (P = 0.21), HDL (P = 0.14)
total cholesterol, high density lipoprotein (HDL) cholesterol, low and BMI (P = 0.54) in MA group were numerically lower, but the
density lipoprotein (LDL) cholesterol and triglycerides (TG), were difference was non-significant. However, the mean serum levels of
measured using enzymatic methods with commercially available LDL (P = 0.02) and CRP (P = 0.047) in patients without MA were
kits (Pars Azmoon, Karaj, Iran). C-reactive protein (CRP), were significantly greater than the MA group (Table 1). FPG, HbA1c, HDL,
measured using the quantitative CRP kit (Pars Azmoon, Karaj, Iran). CRP, BMI, systolic blood pressure, diastolic blood pressure, in both
Serum levels of ICAM-1 were measured using enzyme-linked diabetic groups were significantly higher than the control group
immunosorbent assay (R&D Systems, Minneapolis, Minnesota) (Table 1).
method. At the baseline and follow-up visits, the patients were also Serum levels of ICAM-1 were significantly correlated with age
instructed to collect 24-h urine samples. Completeness of the and HbA1c (Table 2). No significant correlation was detected
collected sample was checked by measuring urinary creatinine between ICAM-1 level with BMI, CRP, and lipid profile (Table 2).
excretion. A repeat measurement was requested if creatinine Results of the comparisons between the three groups are
excretion levels were lower than 20 mg/kg per 24-h and 15 mg/kg demonstrated in Table 3.
per 24-h for men and women, respectively. Urinary albumin
excretion (UAE) was measured by calorimetric methods using 4. Discussion
commercial kits (ZiestChem Diagnostics, Tehran, Iran).
All procedures were conducted in accordance with the guide- Several studies have indicated that serum ICAM-1 concen-
lines of the Helsinki Declaration (2008). Local ethics committee of trations may impact the development of diabetes complications
Tehran University of Medical Sciences approved the study protocol. including nephropathy and retinopathy [18–20,22]. In this study,
In addition, written informed consents were obtained from all serum levels of ICAM-1 in diabetic patients with and without MA
participants before enrollment. were compared; results revealed that serum levels of ICAM-1 were
significantly higher in patients with MA; moreover, it was
2.1. Statistical analysis significantly higher in diabetes patients without MA compared
to the control group. Additionally, this study revealed that serum
Statistical analyses were performed using the SPSS software ICAM-1 levels are significantly associated with age and HbA1c and
package, version 20 for Windows (IBM Corporation, Armonk, New are independent of BMI, CRP, or lipid profile. These findings were in
York). All results are expressed as mean  SD or frequency (N%).
One-way analysis of variance (ANOVA) was used for between-
Table 2
group comparisons of continuous variables, and the chi-square test
Correlation between ICAM-1 and other variables.
was used for categorical variables. Correlations between serum
ICAM-1 concentrations and other variables were estimated by Variables r P-value
Pearson's correlation coefficients. Post-Hoc Tukey test was used to Age 0.21 0.004
compare results between the three groups. In all analyses, a P- SBP 0.32 0.001
DBP 0.13 0.07
value less than 0.05 was considered statistically significant.
FBS 0.17 0.02
HbA1c 0.29 0.001
3. Results Cholesterol 0.002 0.97
HDL 0.06 0.38
Baseline clinical and biochemical characteristics of patients are LDL 0.09 0.19
CRP 0.05 0.43
shown in Table 1. Serum levels of ICAM-1 were significantly higher
BMI 0.07 0.29
in diabetic patients (with or without MA) compared to the healthy
Abbreviations: ICAM-1: intercellular adhesion moleculeSBP: systolic blood pres-
individuals. Moreover, the levels of ICAM in patients with MA were
sure; DBP: diastolic blood pressure; FBS: fasting blood sugar; HbA1c: glycosylated
significantly higher than patients without MA (Table 1). Compari- hemoglobin; HDL: high-density lipoprotein; LDL: low-density lipoprotein choles-
son of patients with and without MA revealed that age and blood terol; CRP: C-reactive protein: BMI: body mass index.
pressure in those with MA were significantly greater than patients

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 Z. Karimi et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 12 (2018) 365–368 367

Table 3
Comparison between controlmicroalbuminuria, and non- microalbuminuria groups.

Group Comparison Mean Difference Std. Error Sig. 95% Confidence Interval

Lower Bound Upper Bound

ICAM Control MA 285.76* 23.03 0.000 340.19 231.33
NMA 66.40* 21.44 0.006 117.08 15.72
MA Control 285.76* 23.03 0.000 231.33 340.19
NMA 219.35* 18.92 0.000 174.64 264.07
NMA Control 66.40* 21.44 0.006 15.72 117.08
MA 219.35* 18.92 0.000 264.07 174.64
FBS Control MA 80.30* 12.37 0.000 109.53 51.07
NMA 98.77* 11.51 0.000 125.98 71.56
MA Control 80.30* 12.37 0.000 51.07 109.53
NMA 18.47 10.16 0.167 42.48 5.54
NMA Control 98.77* 11.51 0.000 71.56 125.98
MA 18.47 10.16 0.167 5.54 42.48
HbA1c Control MA 3.24* 0.27 0.000 3.90 2.58
NMA 3.28* 0.25 0.000 3.90 2.67
MA Control 3.24* 0.27 0.000 2.58 3.90
NMA 0.043 0.22 0.980 0.58 0.49
NMA Control 3.28* 0.25 0.000 2.67 3.90
MA 0.04389 0.22 0.980 0.49 0.58
Cholesterol Control MA 20.62 14.56 0.335 55.04 13.78
NMA 36.88* 13.56 0.020 68.92 4.84
MA Control 20.62 14.56 0.335 13.78 55.04
NMA 16.25 11.96 0.365 44.53 12.01
NMA Control 36.88* 13.56 0.020 4.84 68.92
MA 16.25 11.96 0.365 12.01 44.53
HDL Control MA 6.11 2.63 0.055 0.10 12.32
NMA 2.99 2.44 0.442 2.79 8.77
MA Control 6.11 2.63 0.055 12.32 0.10
NMA 3.12 2.16 0.320 8.22 1.98
NMA Control 2.99 2.44 0.442 8.77 2.79
MA 3.12 2.16 0.320 1.98 8.22
LDL Control MA 5.01 6.41 0.714 10.13 20.17
NMA 12.44 5.97 0.096 26.55 1.66
MA Control 5.01 6.41 0.714 20.17 10.13
NMA 17.46* 5.26 0.003 29.91 5.01
NMA Control 12.44 5.97 0.096 1.66 26.55
MA 17.46* 5.26 0.003 5.01 29.91
CRP Control MA 0.75 0.41 .163 1.73 0.22
NMA 1.46 0.38 0.001 2.38 0.55
MA Control 0.75 0.41 0.163 0.22 1.73
NMA 0.71 0.32 0.073 1.4739 0.05
NMA Control 1.46* 0.38 0.001 0.5522 2.38
MA 0.71 0.32 0.073 0.0504 1.47

Abbreviations: ICAM-1: intercellular adhesion molecule, SBP: systolic blood pressure; DBP: diastolic blood pressure; FBS: fasting blood sugar; HbA1c: glycosylated
hemoglobin; HDL: high-density lipoprotein; LDL: low-density lipoprotein cholesterol; CRP: C-reactive protein: BMI: body mass index.

concert with the results of Ai and Song study which reported that
serum ICAM-1 levels were correlated with the development of
diabetes complications such as retinopathy [22]. Nelson et al. also
indicated that the levels of plasma adhesion molecules are
elevated in patients with type 1 diabetes [16]. Similarly, Bruno
et al. demonstrated similar results indicating that circulating
ICAM-1 is higher in patients with microalbuminuria compared to
those without MA; moreover, it was higher in patients with
normoalbuminuria compared with the control group [23]. Several
studies found that the level of ICAM-1 increases in diabetes and has
a prognostic relationship with albuminuria in patients with T2DM
[24,25]. Serum ICAM levels have also been positively correlated
with albumin/creatinine ratio [25]. Taken together, these studies
have established that diabetic kidney disease is associated with
inflammation, therefore physicians’ attention was drawn to
understanding the impact of inflammation on the pathogenesis
of diabetic nephropathy [26–28]. In addition, in vivo studies on
animals have revealed that leukocyte infiltration is present in all
stages of the development of diabetic nephropathy [29]. Based on
these findings, the authors hypothesized that ICAM-1 plays a
pivotal role in the promotion of macrophage infiltration into the
kidneys, triggering inflammation in renal tissue [26]. It is
suggested that ICAM-1 plays an important role in the pathogenesis
of diabetes. Our study was in agreement with previous findings
and indicated that mean ICAM-1 values in patients with
albuminuria is significantly greater than patients without MA
(531.18  185.84 vs. 311.82  53.82, P = 0.001). In parallel with our
experience, Upadhyay et al. emphasized that in chronic kidney
disease, levels of ICAM -1 is positively correlated to albuminuria
[30], and it is the most important factor in the development and
progression of diabetic nephropathy [31,32]. In general, our
practice supported findings of previous studies and revealed
positive correlation between ICAM-1 and nephropathy.
4.1. Limitations
Several limitations should be considered. First, only serum
ICAM-1 levels were measured and other potential markers (such as
VCAM) related to nephropathy were not evaluated. Second, given
the cross-sectional nature of the study, the results should be
interpreted as exploratory and hypothesis-generating. Third, the
sample size of the study is relatively small. Future prospective
studies on a larger population are warranted to confirm these
findings.

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368 Z. Karimi et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 12 (2018) 365–368
5. Conclusions
This study has shown that Serum levels of ICAM-1 is
significantly higher in diabetic patients with microalbuminuria
but further work needs to be done to establish whether it play a
pivotal role in the pathogenesis of diabetic nephropathy and this
research will serve as a base for them.
Conflicts of interest
The authors declare that there are no conflicts of interest.
Acknowledgements
The authors would like to express their gratitude to the staff
members of Imam Khomeini Hospital for their contribution to the
maintenance of our patient records without which this project
would have been impossible.
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