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                    <p class="art-type" id="articleinfo">Research Article</p>
		    <p class="art-title">Ankle Brachial Index (ABI) measurement associated with High Sensitivity-C-Reactive Protein, Insulin Resistance and Pulse Pressure Levels in Type 2
Diabetes Mellitus Patients</p>
		    <p class="art-author"><?php $authors="Kanokphichayakrai K<sup>1</sup>, Kaewmahanin W<sup>2</sup>, Tangvarasittichai O<sup>3</sup> and Surapon Tangvarasittichai<sup>3*</sup>"; echo (stristr($authors,$coauthor))?str_replace($coauthor,"<a href='".$extpath."authors/".$courl."' target='_blank'>".$coauthor."</a>",$authors):$authors; ?></p>
<p class="art-affl"><sup>1</sup>Division of Echocardiogram, Buddhachinaraj Hospital, Phitsanulok 65000 Thailand<br/>
			 <sup>2</sup>Department of Cadio-Thoracic Technology, Faculty of Allied Health Sciences, Naresuan University, Phitsanulok, 65000 Thailand<br/>
			 <sup>3</sup>Chronic disease research Unit, Department of Medical Technology, Faculty of Allied Health Sciences, Naresuan University,
Phitsanulok, 65000 Thailand</p>
		    <p class="art-aff"><b>*Corresponding author: <?php $corresponding_author="Surapon Tangvarasittichai"; echo ($coauthor!="" && $coauthor==$corresponding_author)?"<a href='".$extpath."authors/".$courl."' target='_blank'>".$coauthor."</a>":$corresponding_author;?></b>,
Associate Professor,
Department of Medical Technology,
Faculty of Allied Health Sciences,
Naresuan University,
Phitsanulok, 65000,
Thailand,
Tel: +66-08-9638-8382,
Fax: +66-0-5596-6300,
E-mail: <a href="mailto:surapon14t@yahoo.com">surapon14t@yahoo.com</a></p>
<p class="art-aff"><b>Received:</b>  February 6, 2018
<b>Accepted:</b>   February 22, 2018
<b>Published:</b> March 1, 2018</p>
<p class="art-aff"><b>Citation:</b> 
 Kanokphichayakrai K, Kaewmahanin W, Tangvarasittichai O, Tangvarasittichai S. Ankle Brachial Index (ABI) measurement associated with High Sensitivity-C-Reactive Protein, Insulin Resistance and Pulse Pressure Levels in Type 2 Diabetes Mellitus Patients. <i>Madridge J Diabetes</i>. 2018; 2(1): 31-35. doi: <a href="https://doi.org/10.18689/mjd-1000106">10.18689/mjd-1000106</a></p>
<p class="art-aff"><b>Copyright:</b> &copy;   2018 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</p>
<p><a href="<?php echo $extpath;?><?php echo $jres['journal_link'];?>/mjd-1000106.pdf" class="btn btn-danger pull-right" target="_blank">Download PDF</a></p>
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<div class="articlecontent">
<p class="art-subhead" id="abstract">Abstract</p>
<p class="art-para">Atherosclerosis is common occurrence in type 2 diabetes mellitus (T2DM) patients.
Peripheral arterial disease (PAD) is a major arteries disease caused by atherosclerosis as
a vascular complication of T2DM. It can be detected by using ankle brachial index (ABI)
measurement. A total of 187 subjects were recruited in present study and underwent
ABI measurement. Thirty one of T2DM patients were abnormal low ABI&le;0.9 (as Gr-1)
and 156 non-T2DM subjects were normal ABI>0.90 (as Gr-2). Comparison of clinical
characteristics of these two groups, Gr-1 were significantly increased in pulse pressure
(PP), dyslipidemia, insulin, insulin resistance (IR) and high sensitivity-C-reactive protein
(hs-CRP) (p<0.05) than Gr-2. Multiple forward stepwise linear regression analyses of the
significant variables showed that in these decreased ABI, independent predictors of
decreased ABI were hs-CRP (&beta; =-0.488, R<sup>2</sup>
 = 0.238, p<0.001), PP (&beta; = -0.320, R<sup>2</sup>
 = 0.336,
p<0.001), triglyceride/high density lipoprotein-cholesterol (TG/HDL-C) ratio (&beta; =-0.279,
R<sup>2</sup>
 = 0.397, p<0.001), IR (&beta; =-0.143, R<sup>2</sup>
 = 0.415, p<0.001), and Age (&beta; = -0.115, R<sup>2</sup>
= 0.428,
p<0.001). In conclusion, abnormal ABI&le;0.9 or PAD is associated with increased PP,
inflammation, IR, dyslipidemia and age. ABI measurement is a useful tool to estimate
PAD and cardiovascular diseases risk marker in asymptomatic patients.</p>

<p class="art-para"><b>Keywords:</b> Ankle brachial index; Peripheral arterial disease; Atherosclerosis; Highsensitivity C-reactive protein; Pulse pressure; Insulin resistance.</p>

<p class="art-subhead" id="intro">Introduction</p>
<p class="art-para">Atherosclerosis progression is the process affected by the alteration of vascular
endothelial cell beds with clinically demonstrated life threatening consequences
including coronary artery disease (CAD), cerebrovascular disease, and peripheral arterial
disease (PAD) <a href="#1" id="ref1">[1]</a>. Peripheral arterial disease is one of the common evidence of
atherosclerosis. The prevalence of PAD was increased with age, hypertension, diabetes
and smoking <a href="#2" id="ref2">[2</a>-<a href="#5" id="ref5">5]</a>. People with PAD often have lower extremity circulation problems
and they are at higher risk for both cardiovascular disease (CVD) and cerebrovascular
disease event <a href="#2" id="ref2">[2]</a>. Peripheral arterial disease is commonly assessed by using ankle
brachial systolic blood pressure index (ABI) measurement <a href="#6" id="ref6">[6</a>, <a href="#7" id="ref7">7]</a>. The ABI result is the
ratio of Doppler- or sphygmomanometry-determined lower extremity blood pressure
to brachial artery blood pressure. Reproducibility of the ABI measurement is good with the mean error of 8-9% within or between measurements <a href="#8" id="ref8">[8]</a>.
Peripheral arterial disease severity is assessed according to
the levels of ABI: (i) 0.91-1.30: normal, (ii) 0.70-0.90: mild
occlusion, (iii) 0.40-0.69: moderate occlusion, (iv) <0.40:
severe occlusion and (v) >1.30: poorly compressible vessels.
The American Diabetes Association recommends measuring
ABI in all adults older than 50 years and history of smoking,
hypertension or diabetes or in any patient having PAD and
other CV risk factors <a href="#9" id="ref9">[9]</a>.</p>

<p class="art-para">C-reactive protein (CRP) is an inflammation marker
recommended for risk assessment for primary prevention of
cardiovascular disease <a href="#10" id="ref10">[10</a>, <a href="#11" id="ref11">11]</a>. Increased CRP level is associated
with increased risk of cardiovascular disease <a href="#12" id="ref12">[12]</a> and increased
vascular stiffness can be caused by atherosclerosis and aging.</p>
<p class="art-para">Age related increases in blood pressure (BP) usually show
the systolic blood pressure (Syst) elevation while maintaining
or having a slight decrease in a diastolic BP. This induces in
the widening of pulse pressure (difference of systolic and
diastolic blood pressure) <a href="#13" id="ref13">[13]</a>. However, BP can be divided
into two components: (i) steady (mean arterial pressure; MAP)
and (ii) pulsatile (pulse arterial pressure, PP) <a href="#14" id="ref14">[14]</a>. Previous
research has linked elevated PP (estimate of arterial stiffness)
with a higher risk of cardiovascular morbidity and mortality
<a href="#15" id="ref15">[15</a>, <a href="#16" id="ref16">16]</a>. Arterial hypertension (steeper age-related widening
of PP) also promotes vascular stiffness <a href="#17" id="ref17">[17]</a>. High peripheral
resistance is the hallmark of arterial hypertension, but always
exerts hemodynamic changes that could counteract the effect
of the increase in MAP on PP. In this regard, peripheral
resistance maintains a reciprocal relationship with stroke
volume and PP <a href="#18" id="ref18">[18]</a>. In the present study, we aim to
demonstrate that PAD (ABI<0.9) is associated with increased
PP, inflammation, IR, dyslipidemia and age. ABI measurement
can use as the tested tool to estimate subclinical atherosclerosis
and CVD risk in patients with PAD.</p>

<p class="art-subhead" id="method">Methods</p>
<p class="art-para"><b>Study Population</b><br/>
Two hundred and five of female participants from the
Cardiovascular Diseases in Diabetes Patients Project during
October 2012-December 2013 were used in the present
study. Volunteers were excluded, if they had an ongoing
febrile illness, history of a connective tissue disorders, non-atherosclerotic arterial disease, history of lower extremity
bypass or percutaneous angioplasty in the preceding year
and those with an ABI >1.3 caused by poorly compressible
arteries in the lower extremities. Eighteen participants didn't
participate in ABI measurement section was excluded from
the study. The number of eligible participants was 187 in the
present study. Thirty one subjects with T2DM were identified
as PAD with abnormal low ABI &le;0.9(Gr-1) and 156 subjects
without T2DM were identified as without PAD with normal
ABI &gre;0.9(Gr-2). The research protocol was approved by the
Ethics Committee of the Naresuan University. All participants
gave informed consent before their provided blood samples
and underwent assessment for ABI measurement.</p>

<p class="art-para"><b>Anthropometric, Blood Pressure and ABI Measurements</b><br />
Questionnaires were used to record clinical characteristics
including diagnosis of hypertension, diabetes, a history of MI
or stroke, smoking, alcohol use, and medications of each
participant at the study visit. Anthropometric measurements
of the study included height; weight and waist circumference
(WC).The body mass index (BMI) was calculated from height
and weight as kg/m<sup>2</sup>. Blood pressure (BP) was measured by
using Omron HEM-7080 (Omron Health care, Tokyo, Japan).
Pulse pressure (PP) was determined by subtracting the diastolic
from the systolic blood pressure (Syst), and mean arterial
pressure (MAP) was calculated by using the formula: [(systolic
blood pressure) + (2 x diastolic blood pressure)]/3 <a href="#19" id="ref19">[19]</a>.</p>
<p class="art-para">Ankle brachial index measurement is made in the supine
position after 5 min of rest by using Sphygmanometer and
Sphygmograph (Vasera, VS-1500N ver. 04; Fukuda Denshi,
Japan). A pneumatic-cuff is placed around the ankle and the
pressure is measured at both the dorsalis pedis and posterior
tibial arteries using a hand held continuous wave Doppler
probe (5-10 MHz). We used the same technique measurement
in both arms for brachial artery pressure. The higher of the
two ankle pressures is divided by the brachial artery pressure.
In subjects with normal lower limb arterial circulation, the
systolic pressure at the ankle is usually 10-15 mmHg higher
than the arm measurement, it caused from pulse wave velocity
<a href="#20" id="ref20">[20]</a>, resulting in an ABI >1.10. Following the recommendation
of the International medical societies for the ABI calculation,
the highest pressure in the leg is divided by the highest
pressure in the arm <a href="#9" id="ref9">[9</a>, <a href="#21" id="ref21">21</a>-<a href="#22" id="ref22">22]</a>. Reproducibility of the ABI
measurement seemed to be good. In the ABI study, the mean
error of 8-9% within or between observers is smaller than with
established screening measures <a href="#8" id="ref8">[8]</a>. The lower of the resting
ABI values for the right and left arms and legs was used in the
analyses involving the ABI. PAD was defined as an ABI &le; 0.9 in
both arms and legs.</p>
<p class="art-para"><b>Blood Sample Collection and Biochemical Determination</b><br/>
Fasting venous blood was collected from all participants.
Plasma glucose (Glu), blood urea nitrogen (BUN), total
cholesterol (TC), triglycerides (TG) and high density lipoprotein
cholesterol (HDL-C) were measured by enzymatic method
(Roche diagnostic, Switzerland). Serum creatinine (CT) level
was determined based on the Jaffe reaction. LDL-C level was
calculated with Friedewald's formula in specimens with TG
level<400 mg/dl.</p>
<p class="art-para"><b>Highly Sensitive C - reactive protein (hs-CRP) Assay</b><br/>
Highly sensitive-CRP concentrations were determined by
using latex particle enhanced immune turbid metric assay on
the Hitachi 912 auto-analyzer (Roche Diagnostic, Switzerland)
that has been standardized against the World Health
Organization reference. The normal range of hs-CRP was<3.0
mg/l (<0.03 g/l).</p>
<p class="art-para"><b>Insulin Assay</b><br>
Fasting insulin levels were measured based on micro-particle enzyme immunoassay (MEIA) technology using Abbott
reagents with Axsym system (Abbott laboratories, Illinois, USA). All participants underwent evaluation of insulin resistance
index (IR) by using the Homeostasis model assessment
(HOMA)-formula <a href="#23" id="ref23">[23]</a>. HOMA of insulin resistance (IR) was
defined using the following formula: fasting glucose (mmol/l) x
fasting insulin (&micro;U/ml)/22.5 <a href="#23" id="ref23">[23]</a>.</p>

<p class="art-para"><b>Statistical Analysis</b><br/>
All data were expressed as median and inter quartile range,
and compared the differences between groups by using the
Mann-Whitney <i>U</i>-test. Spearman rank correlation was used to
assess the correlation of all clinical markers in the study
participants. Clinical variables that correlated with PAD (ABI) in
the present study were tested as independent variables by
using multivariate forward stepwise linear regression analysis.
Tests were two tailed, and a <i>p</i>-value<0.05 was considered
significant. All analyses were performed using the SPSS
statistical package, version 13.0 (SPSS Inc., Chicago, IL, USA).</p>

<p class="art-subhead" id="result">Results</p>
<p class="art-para">General characteristics of both groups were demonstrated in
Table 1. In the comparison of clinical characteristics of both groups,
Gr-1 demonstrated more difficult physical activity, significantly
greater PP, TC, TG, hs-CRP, insulin, IR,TG/HDL-C ratio and lower
HDL-C levels than Gr-2. Bivariate correlations, ABI was significantly
correlated with Syst (r=-0.384, p<0.001), PP (r=-0.437, p<0.001),
MPP (r=-0.238, p<0.001), TC (r=-0.326, p<0.001), hs-CRP
(r=-0.388, p<0.001), insulin (r= -0.269, p<0.001), IR (r=-0.287,
p<0.001) and TG/HDL-C ratio (r=-0.299, p<0.001). The correlation
of the other clinical variables was shown in Table 2. We used
multiple forward stepwise linear regression analysis to examine
effects of variables in the association of these variables with ABI.
Statistics were listed in Table 3. Hs-CRP, PP, TG/HDL-C ratio, IR and
age showed the association with ABI, which remained highly
significant after adjusting for any clinical or laboratory confounding
variables [hs-CRP (&beta; = -0.488, R<sup>2</sup>
 = 0.238, p<0.001), PP (&beta; = -0.320,
R<sup>2</sup>
 = 0.336, p<0.001), TG/HDL-C ratio (&beta; = -0.279, R<sup>2</sup>
 = 0.397,
p<0.001), IR (&beta; = -0.143, R<sup>2</sup>
 = 0.415, p<0.001) and Age (&beta; = -0.115,
R<sup>2</sup>
 = 0.428, p<0.001)].</p>

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<img src="<?php echo $imgpath;?>images/mjd-106-t002.gif" class="img-responsive center-block"/></div>
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<img src="<?php echo $imgpath;?>images/mjd-106-t003.gif" class="img-responsive center-block"/></div>


<p class="art-subhead" id="discussion">Discussion</p>
<p class="art-para">The risk of atherosclerotic disease is markedly increased
among individuals with diabetes, hypertension and aging.
Atherosclerosis is the major cause of the death and disability
in these subjects <a href="#24" id="ref24">[24]</a>, PAD disease is a common evidence of
atherosclerosis that share the common risk factors. General
characteristic of PAD is usually caused occlusive arterial
vessels of the lower extremities, but many are asymptomatic <a href="#25" id="ref25">[25]</a>. The loss of function and long-term disability progression
reduced walking speed and distance associated with
intermittent claudicating <a href="#9" id="ref9">[9</a>, <a href="#26" id="ref26">26]</a>, subjects with low ABI<0.9
were a sign of severe atherosclerosis in their arms and legs.
Our data supports these PAD patients showing increased PP,
TC, TG, TG/HDL-C ratio, hs-CRP, insulin, IR, reduced HDL-C
and older age.PAD (low ABI&le;0.9)patients were demonstrated
higher hs-CRP; an inflammation marker, is a major component
and plays the major role in atherosclerosis <a href="#10" id="ref10">[10</a>,<a href="#27" id="ref27">27]</a>. Increased
PP may indicate PAD patients are at high risk in for morbidity
and mortality from CVD. Pulse pressure reflects vascular
stiffness of the aorta and large arteries and pulse wave velocity
that may be cause by atherosclerosis and aging <a href="#28" id="ref28">[28]</a>. An
increased PP is associated with the development of left
ventricular dysfunction and clinical heart failure in the
hypertensive and elderly <a href="#29" id="ref29">[29]</a>. PAD (low ABI&le;0.9) patients
were also demonstrated insulin resistance state, decrease
insulin function and insulin ability to inhibit lipolysis leads to
increase FFAs generation and decrease lipoprotein lipase
activity. This generates a chylomicron remnant rich in TG <a href="#30" id="ref30">[30]</a>,
caused elevated hepatic FFAs and VLDL TG-rich particles
secretion. These processes also generate HDL particles
containing high TG concentrations. This HDL-C high TG
containing is hydrolyzed with hepatic lipase to produce TG
and smaller HDL that less antiatherogenic activity and easily
to remove from the body by the kidney and caused higher
TG/HDL-C ratio. Thus, both insulin resistance and dyslipidemia
associated with endothelial damage led increased risk of CVD
<a href="#31" id="ref31">[31]</a> in these PAD (low ABI) patients. Our present study
demonstrated the same as Lee et al. <a href="#32" id="ref32">[32]</a> reported association
of ABI and the development of diabetic retinopathy, similar to
PAD, and the study of Subramaniam et al. <a href="#33" id="ref33">[33]</a> demonstrated
ABI measurement as a marker for CVD assessment in multiethnic. Previous studies have been demonstrated PAD
patients or abnormal low ABI was associated with enlarge of
plaques in aortic arch <a href="#34" id="ref34">[34]</a>, arterial stiffness (increased PP) and
aortic calcification <a href="#35" id="ref35">[35]</a>.</p>
<p class="art-para">PAD is often referred to as an under-diagnosed and
under-treated public health problem. There are the practice
guidelines from the American College of Cardiology/
American Heart Association for the management of PAD
patients. They recommend all asymptomatic adult age &ge;50
year-olds to measure ABI, especially those with current or
history of smoking, diabetes and hypertension, also in adults
with lower extremity circulation problems and age &ge;70 years
old should be assess for early CVD prevention and treatment
<a href="#2" id="ref2">[2]</a>. ABI measurement is a non-invasive test for atherosclerosis
detection. Therefore, routine screening for PAD has been
advocated in these adults using ABI measurement. Limitations
of the present study were use of cross-sectional data, a
relatively small patient sample size and one district. Subjects
had only one time ABI measurement.</p>

<p class="art-subhead" id="conclusion">Conclusion</p>
<p class="art-para">ABI (or PAD) measurement should be considered as the
tool for CVD risk assessment and atherosclerosis risk marker.
The ABI measurement is a simple, cheap, noninvasive and
reliable as the tested tool and could help the clinicians to
diagnose PAD and atherosclerosis risk.</p>

<p class="art-subhead" id="ack">Acknowledgement</p>
<p class="art-para">We sincerely thank the Cardiovascular and Diabetes
Prevention in Elderly Project of Faculty of Allied Health
Sciences for financial support to this study. We wish to thank
all co-workers for their blood collection and technical
assistance. We particularly thank the patients who participated
in this study and Asst. Prof. Dr. Ronald A. Markwardt, Burapha
University, for his critical reading and correcting of the
manuscript.</p>

<p class="art-subhead" id="conflict">Conflict of interest</p>
<p class="art-para">The authors have no conflict of interest to report.</p>

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            </div>
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<?php include 'includes/jrnfooter.php';?>

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