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                    <p class="art-type" id="articleinfo">Research Article</p>
		    <p class="art-title">Morpho-Anthropological characteristic of the distribution of Adipose Connective Tissue in Elderly Bulgarian Males with Type 2 Diabetes Mellitus</p>
		    <p class="art-author"><?php $authors="Atanas Baltadjiev<sup>*</sup>"; echo (stristr($authors,$coauthor))?str_replace($coauthor,"<a href='".$extpath."authors/".$courl."' target='_blank'>".$coauthor."</a>",$authors):$authors; ?></p>
<p class="art-affl">Department of Anatomy, Histology and Embryology, Faculty of Medicine, Medical University-Plovdiv, Bulgaria</p>
		    <p class="art-aff"><b>*Corresponding author: <?php $corresponding_author="Atanas Baltadjiev"; echo ($coauthor!="" && $coauthor==$corresponding_author)?"<a href='".$extpath."authors/".$courl."' target='_blank'>".$coauthor."</a>":$corresponding_author;?></b>,
Associate Professor,
Department of Anatomy, Histology and
Embryology,
Faculty of Medicine,
Medical University of Plovdiv,
15A Vassil Aprilov Blvd,
4002 Plovdiv,
Bulgaria,
Tel: +359886359609,
E-mail: <a href="mailto:dr_atanas@abv.bg">dr_atanas@abv.bg</a></p>
<p class="art-aff"><b>Received:</b>   May 16, 2018
<b>Accepted:</b>     June 4, 2018
<b>Published:</b>  June 9, 2018</p>
<p class="art-aff"><b>Citation:</b> Baltadjiev AG. Morpho-Anthropological
characteristic of the distribution of Adipose
Connective Tissue in Elderly Bulgarian Males
with Type 2 Diabetes Mellitus. <i>Madridge J Diabetes</i>. 2018; 2(1): 42-46.
doi: <a href="https://doi.org/10.18689/mjd-1000108">10.18689/mjd-1000108</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-1000108.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"><b>Background:</b> Diabetes is becoming a rapidly growing health concern across the world
due to rapidly growing number of patients. Obesity and type 2 Diabetes Mellitus (T2DM)
are closely related.<br/>
The aim of this study was to investigate the distribution of adipose connective tissue
in elderly Bulgarian male patients with T2DM.</p>
<p class="art-para"><b>Patients and Methods:</b> Subjects of the research were 97 men suffering from T2DM, with
age range 60-80 years. The control group included 40 Bulgarian healthy men in the same
age range. Directly measured parameters: body height, body weight, 9 skinfolds (sf) and
Bioelectrical Impedance analysis. Calculated indexes: Body mass index (BMI), the ratio
sfTrunk/sfLimbs, the ratio skin folds upper half of body/skin folds lower half of body, fat
mass and subcutaneous fat mass.</p>
<p class="art-para"><b>Results:</b> Statistically significant differences were found among the means of body weight,
sfXrib, sfThigh, BMI, % body fat tissue, visceral fat tissue, fat mass and subcutaneous fat
mass between the diabetic and healthy men. The body composition of elderly male
patients with diabetes contained a significant larger adipose component than the controls.
The well expressed visceral adipose tissue which determines the body composition is a
reliable <i>indicator</i> of the health risks in elderly patients with T2DM.</p>
<p class="art-para"><b>Conclusion:</b> In male patients with T2DM aged 60-80 years the model of subcutaneous
adipose tissue distribution was predominant in the upper torso region and less in the
limbs. The common fat tissue and visceral adipose tissue in male patients were significantly
more expressed than the healthy controls. These data revealed a worse anthropological
status of the body composition in male patients with T2DM.</p>

<p class="art-para"><b>Keywords:</b> Type 2 diabetes mellitus; Elderly males; Adipose tissue; Skinfolds.</p>

<p class="art-subhead" id="intro">Introduction</p>
<p class="art-para">Type 2 Diabetes mellitus (T2DM) is a metabolic disease associated with disturbance
of the metabolism. In recent years, it is gaining more signs of social problem due to the
rapidly growing number of people affected by the disease worldwide. As of 2015, it was
estimated that 415 million people had diabetes worldwide, with type 2 DM making
about 90% of those cases. This represents 8.3% of the adult population, with equal rates
in both women and men. According to the International Diabetes Federation, the
number of diabetes mellitus patients in Europe is expected to increase from 52 millions
in 2014 to 68.9 millions by 2035, mostly due to increases in overweight and obesity,
unhealthy diet and physical inactivity <a href="#1" id="ref1">[1]</a>. According to WHO this is about 10.3% of men and 9.6% of women aged 25 years and over (Today's
Market Study of Diabetes, https://www.diabetesexpo.com/
europe/). Across Europe, about 1 in 11 adults is affected and
this number is set to rise as the population ages. In Bulgaria
around 8-9% of the population suffers from this disease.</p>

<p class="art-para">Most of the researchers are interested in etiology,
pathogenesis, clinical course and treatment of the disease.
The anthropological status of patients with diabetes takes
little attention. The fat accumulation in the body of patients
with diabetes occurs primarily in two locations: in the
abdomen (central, abdominal, visceral) and subcutaneously
(peripheral). Fat accumulation in the abdominal area is
commonly associated with increased risk for T2DM <a href="#2" id="ref2">[2</a>, <a href="#3" id="ref3">3</a>, <a href="#4" id="ref4">4</a>, <a href="#5" id="ref5">5]</a>.
Not many studies have been performed for the subcutaneous
distribution of adipose connective tissue. World literature
offers little data on the complex deposition of adipose
connective tissue in patients with T2DM. The purpose of this
study was to investigate the distribution of adipose tissue in
61-80 years old Bulgarian male patients with T2DM.</p>

<p class="art-subhead" id="method">Subjects and Methods</p>
<p class="art-para">137 men were enrolled in the study. Subjects of the study
were 97 men with T2DM and 40 healthy men (controls). They
were diagnosed by a <i>diabetes specialist</i> and recruited from
the Clinic of endocrinology of St.George University Hospital
at the Medical University of Plovdiv, Bulgaria. The study
period was 2009-2014.</p>
<p class="art-para">The inclusion criteria were: Bulgarian ethnicity, duration
of the disease of not less five years, clinically compensated
diabetes at the time of the study, age range 60-80 years
(mean 68.75&plusmn;0.58 SEM yrs). The control group included 40
men at the same age range (mean 69.76&plusmn;0.90 SEM yrs).</p>
<p class="art-para">The exclusion criteria were: previous or existing
metabolic, oncological and other disorder that could
compromise the anthropological study: thyroid related
diseases, adrenal glands related diseases, cancer etc. The
anthropological methods included:</p>
<p class="art-para"><b>Directly measured parameters</b><br/>
Body height and body weight, skinfold (sf) thicknesses
were measured at 9 locations-sfTriceps, sfBiceps (brachii),
sfForearm, sfSubscapular, sfXrib, sfAbdomen, sfSuprailiaca,
sfThigh, and sfCalf, using Harpenden Skinfold Calipers (British
Indicators Ltd) at standard sites on the right side of the body.</p>

<p class="art-para"><b>Bioelectrical Impedance Analysis (BIA)</b><br/>
-% body fat tissue and visceral fat tissue - was measured
with a Body Composition Monitor Tanita.BC-532.
</p>
<p class="art-para"><b>Calculated Indexes</b><br/>
Body mass index (BMI); sfTrunk/sfLimbs ratio; skinfolds
upper half of body/skinfolds lower half of body ratio; fat mass
and subcutaneous fat mass.</p>
<p class="art-para"><b>Statistical Analysis</b><br/>
Data were analyzed using statistical software SPSS version
15 (SPSS Inc., Chicago, IL). <i>Parametric statistical</i> methods
were relevant. Independent Samples <i>t</i> Test was used to
compare the means of two <i>independent</i> anthropologic
parameters in order to determine whether there was
statistical evidence that the means were significantly
different. The one-way analysis of variance (<i>ANOVA</i>) was
used to determine whether there were any significant
differences between the means of three or more
independent parameters. P&lt;0.05 (two tailed) was considered
statistically significant. We used Pearson's correlation to
assess associations between variables, and Pearson's
correlations coefficient (PC) was calculated. The value of the
coefficient was used to rate the correlation's strength: low
correlation - 0.01-0.30; moderate - 0.30-0.50; strong 0.50-0.70; high - 0.70-0.90; very high >0.90. P<0.05 (two tailed) was
considered statistically significant.
</p>

<p class="art-subhead" id="result">Results</p>
<p class="art-para">In the present study significant differences were found
between the means of weight. The mean value of the male
patients with diabetes was higher than the controls. The
difference was very well expressed (p<0.001).</p>
<p class="art-para">No statistical difference was detected among the
thicknesses of sfTriceps (brachii) between the male patients
with diabetes and the controls (p>0.05). The sfTriceps (brachii)
of the diabetic patients was significantly thicker in comparison
to the sfBiceps, sfForearm and sfCalf, but significantly thinner
than sfSubscapular, sfXrib, sfSuprailiaca, sfAbdomen and
sfThigh in the same group (<i>ANOVA</i>, p<0.001). The correlation analysis revealed many positive correlations between the thicknesses of sfTriceps and other skinfolds, as follows: the correlations were high to sfBiceps (r=0.76); strong to
sfSubscapular, sfXrib, sfSuprailiaca, sfAbdomen, sfThigh and
sfForearm (r=0.50-0.70), and moderate to sfCalf (r=0.41).</p>

<p class="art-para">No statistically significant difference was found between
the thicknesses of sfSubscapular in the diabetic male patients
in comparison to the controls (p>0.05). The sfSubscapular of
the diabetic patients was significantly thicker in comparison
to the sfTriceps, sfSuprailiaca, sfBiceps, sfForearm, sfThigh
and sfCalf of the same men (<i>ANOVA</i>, p<0.001). At the same
time sfSubscapulare was significantly thinner than sfAbdomen
(p<0.001). The correlation analysis revealed a lot of positive
significant correlations between the thicknesses of
sfSubscapular and other skinfolds, as follows: high correlations
to sfSuprailiaca and sfAbdomen (r=0.70-0.90); strong
correlations to sfXrib, sfTriceps, sfBiceps, sfForearm and
sfThigh (r=0.50-0.70), and moderate correlations to sfCalf
(r=0.34).</p>

<p class="art-para">The thickness of sfXrib in the elderly diabetic male
patients was significantly higher than the healthy controls.
The difference was statistically significant (p<0.001). The
sfXrib of the diabetic patients was significantly thicker
compared to sfTriceps, sfBiceps, sfForearm, sfSuprailiaca,
sfThigh and sfCalf of the same men, but it was thinner than
sfAbdomen (<i>ANOVA</i>, p<0.001). The correlation analysis
revealed many positive significant correlations between the thicknesses of sfXrib and other skinfolds, as follows: strong
correlations to sfSubscapular, sfSuprailiaca, sfAbdomen and
sfTriceps (r=0.50-0.70); moderate to sfBiceps, sfForearm,
sfThigh and sfCalf (r=0.30-0.50).</p>
<p class="art-para">We didn't detect any statistically significant difference
among the thicknesses of sfSuprailiaca between the diabetic
male patients and healthy controls (p>0.05). The sfSuprailiaca
of diabetic patients was thicker in comparison to sfTriceps,
sfBiceps, sfForearm and sfCalf of the same men, but it was
thinner than sfSubscapular, sfXrib, sfAbdomen and sfThigh
(<i>ANOVA</i>, p<0.001). The correlation analysis revealed many
positive correlations between the thicknesses of sfSuprailiaca
and other skinfolds, as follows: high correlations to
sfSubscapular and sfAbdomen in the same topographical
area (r=0.70-0.90), and strong correlations to other skinfolds
(r=0.50-0.70).</p>

<p class="art-para">No statistically significant difference was found among
the thicknesses of sfAbdomen between the male patients
with diabetes and healthy controls (p>0.05). It was the thickest
skinfold among all studied skinfolds in the diabetic patients
and the difference was very well expressed (<i>ANOVA</i>, p<0.001).
The correlation analysis revealed many positive correlations
between the thicknesses of sfAbdomen and other skinfolds,
as follows: high correlation to sfSuprailiaca and sfSubscapular
(r=0.70-0.90); strong - to sfXrib, sfTriceps, sfForearm, sfThigh
and sfCalf (r=0.50-0.70), moderate - to sfBiceps (r=0.47).</p>
<p class="art-para">There was no statistically significant difference between
the thicknesses of sfBiceps in the elderly male patients in
comparison to the controls (p>0.05). The sfBiceps was the
thinnest skinfold in comparison to other studied skinfolds
(<i>ANOVA</i>, p<0.05). The mean value of sfBiceps of diabetic
patients was lower compared to sfForearm, but without
significant difference (p>0.05). At the same time, we found
that the thickness of sfForearm was significant higher than
sfBiceps in the group of healthy men (p<0.05). The correlation
analysis revealed many positive significant correlations to the
thicknesses of the other studied skinfolds. The correlations
were high to sfForearm and sfTriceps (r=0.70-0.90); strong -
to sfSubscapular and sfSuprailiaca (r=0.50-0.70); moderate to
sfXrib, sfAbdomen, sfTriceps and sfThigh (r=0.30-0.50); low to
sfCalf (r=0.23).</p>

<p class="art-para">There was no statistically significant difference between
the thicknesses of sfForearm between the male patients with
diabetes and healthy controls (p>0.05). The sfForearm was
significant thinner than other investigated skinfolds, except
sfBiceps. The correlation analysis revealed several positive
significant correlations of the sfForearm thickness to the other
skinfolds (p<0.001). The correlations were high to sfBiceps
(r=0.75); strong to sfTriceps, sfSubscapular, sfSuprailiaca,
sfAbdomen and sfThigh (r=0.50-0.70); moderate to sfXrib and
sfCalf (r=0.30-0.50).</p>
<p class="art-para">The thickness of sfThigh in the elderly male patients with
diabetes was significantly lower than the controls (p<0.05). It
was significantly thicker in comparison to the sfTriceps,
sfBiceps, sfForearm and sfCalf, but significantly thinner than
sfSubscapular, sfXrib and sfAbdomen (<i>ANOVA</i>, p<0.05). The correlation analysis revealed many positive correlations
between the thickness of sfThigh and other studied skinfolds
(p<0.05). The correlations were strong - to sfSubscapular,
sfSuprailiaca, sfAbdomen, sfTriceps, sfForearm and sfCalf
(r=0.50-0.70); moderate - to sfBiceps and sfXrib (r=0.30-0.50).</p>
<p class="art-para">We didn't detect any statistically significant difference
among the thicknesses of sfCalf between the male patients
with diabetes and healthy controls (p>0.05). It was significantly
thicker than sfBiceps and sfForearm, but it was significantly
thinner than other studied skinfolds (<i>ANOVA</i>, p<0.001). The
correlation analysis revealed several positive correlations
between the sfCalf thickness and other skinfolds (p<0.05).
The correlations were strong to sfSuprailiaca, sfAbdomen and
sfThigh (r=0.50-0.70); moderate to sfSubscapular, sfXrib,
sfTriceps and sfForearm; low to sfBiceps(r=0.23).</p>

<div class="art-img">
<img src="<?php echo $imgpath;?>images/mjd-108-t001.gif" class="img-responsive center-block"/></div>
<p class="art-para">The accumulation of subcutaneous adipose tissue in
elderly patients with Type 2 diabetes mellitus was higher in
the torso, than in the limbs. In contrast, the controls exhibited
an opposite distribution. In patients with Type 2 diabetes
mellitus the accumulation of subcutaneous adipose tissue
was larger in the upper half of the body, than in the lower half.
The controls exhibited the opposite distribution it was
statistically significant as demonstrated in Table 2.</p>
<div class="art-img">
<img src="<?php echo $imgpath;?>images/mjd-108-t002.gif" class="img-responsive center-block"/></div>

<p class="art-para"><b>Body Composition Parameters' Results, Investigated by
Bioelectrical Impedance Analysis</b><br/>
The BMI of the elderly male patients suffering from
diabetes was significantly higher than that of the healthy
controls (p<0.05). This index demonstrates a total deposition
of adipose tissue in the human body. The values of the %
body fat tissue of patients with diabetes were significantly higher than the controls (p<0.05). The values of visceral fat
tissue were significantly higher in the patients, than in the
controls (p<0.05). The mean value of fat mass in the male
patients was significantly higher than in the healthy controls
(p<0.001). The mean value of subcutaneous fat tissue was
significantly higher in the patients with diabetes than in the
healthy controls (p<0.001).</p>
<div class="art-img">
<img src="<?php echo $imgpath;?>images/mjd-108-t003.gif" class="img-responsive center-block"/></div>



<p class="art-subhead" id="discussion">Discussion</p>
<p class="art-para">This study is part of a complex survey involving T2DM
male patients 40-60 years, 60-80 years, as well as female
patients from both age groups in Bulgaria. The anthropological
parameters provide a large data base, specific for Bulgarian
population. Using the anthropological parameters it will be
possible to calculate the components of the somatotype by
Heath and Carter method of somatotyping, as well as other
indexes. They will reveal the anthropological status of
Bulgarian patients with T2DM.</p>
<p class="art-para">It has been found that abdominal obesity, also known as
central or visceral obesity, was more closely related to T2DM
than the general obesity. The visceral fat is more metabolically
active and produces more insulin resistance <a href="#6" id="ref6">[6</a>, <a href="#7" id="ref7">7</a>, <a href="#8" id="ref8">8</a>, <a href="#9" id="ref9">9]</a>. Similar
data were observed in Bulgarian men aged 60-80, with a
diagnosis T2DM. The values of the "% fat mass", "visceral
adipose tissue" and "adipose tissue-FM" were statistically
higher in the elderly male patients with T2DM than in the
healthy controls, demonstrated in table 3. It was considered
that this type of obesity increased the risk of pathological
changes in other systems, along with the progress of T2DM
<a href="#10" id="ref10">[10</a>, <a href="#11" id="ref11">11</a>, <a href="#12" id="ref12">12</a>, <a href="#13" id="ref13">13]</a>.</p>
<p class="art-para">Attention should be paid to the distribution of subcutaneous
adipose tissue in patients with T2DM. Two significant differences
were detected among the thicknesses of sfXrib and sfThigh
between the elderly male patients and the healthy controls in
this study. The skinfold thickness of Xrib in the patients with
diabetes was significantly higher than the controls, but the
skinfold thickness of Thigh in the healthy controls was
significantly greater than the elderly patients, demonstrated in
table 1. The common subcutaneous fat mass was significantly
higher in the patients with diabetes than the controls. This
difference was statistically significant (p<0.001), demonstrated
in table 3. It was found that in patients with T2DM the
accumulation of subcutaneous adipose tissue was primarily in
torso and less in the limbs. The accumulation of adipose tissue
consisted predominantly in the upper body as compared to the
lower, the so-called &bdquo;apple shaped", demonstrated in table 2. These patients have a worse anthropological status, that would
lead to more severe clinical course of the disease <a href="#14" id="ref14">[14</a>, <a href="#15" id="ref15">15</a>, <a href="#16" id="ref16">16</a>, <a href="#17" id="ref17">17]</a>. In controls the deposition of adipose tissue was
predominantly in the limbs and mainly in the lower part of the
body, the so-called &bdquo;pear shaped". It can be assess by
measurement of skin folds. This study revealed a lot of positive
correlations among the skinfolds thicknesses. An interest
induced the data indicating that skinfolds from topographically
neighboring areas were in a stronger correlation with each
other, than did skin folds from distant topographical areas.
Some authors have reported the importance of adipose tissue
accumulation in the anterior abdominal wall <a href="#18" id="ref18">[18]</a>. In this
investigation the sfAbdomen was the thickest, compared to the
other studied skinfolds in patients with T2DM, but it was not
detected a significant difference compared to the thickness of
the corresponding skinfold in the controls. Significantly greater
skinfold thickness was measured in the control group than in
the corresponding skinfolds in patients with T2DM, as
happened with sfThigh only. These facts confirmed the greater
importance of the accumulation of visceral fat than of
subcutaneous fat for the prognosis of disease <a href="#19" id="ref19">[19</a>, <a href="#20" id="ref20">20</a>, <a href="#21" id="ref21">21]</a>.</p>
<p class="art-para">Total weight and BMI were higher in patients with
diabetes than the controls (p<0.05). Men with T2DM were
overweight and obese compared to healthy controls, but
these values had less importance for the prognosis of disease
compared with the above described parameters. <a href="#22" id="ref22">[22</a>, <a href="#23" id="ref23">23</a>, <a href="#24" id="ref24">24]</a>.
More original data about the anthropological status of
Bulgarian patients with T2DM were published in other our
publications <a href="#25" id="ref25">[25]</a>.</p>

<p class="art-subhead" id="conclusion">Conclusion</p>
<p class="art-para">The body composition of elderly diabetic male patients
with T2DM aged 60-80 years contained a larger common
adipose component than the controls. The values of weight
and BMI in the patients with diabetes were significantly higher
than the controls.</p>
<p class="art-para">The subcutaneous adipose tissue was accumulated
mostly in the upper part of the torso in the patients with
diabetes, opposite - in the group of healthy men (controls),
the subcutaneous adipose tissue was accumulated mostly on
the lower part of the body. In the group of elderly patients
with diabetes the subcutaneous adipose tissue was
accumulated predominant in the torso, than in the peripheral
part of the body (arms, thighs and lower legs). The thickness
of sfXrib in the diabetic patients was significantly higher than
in the controls, but sfThigh was significantly thinner than the
controls.</p>
<p class="art-para">The bioelectrical impedance analysis of the body composition
demonstrated that the common fat tissue and visceral adipose
tissue in male patients suffering from T2DM was significantly
more expressed than the healthy controls. These data revealed a
worse anthropological status of the body composition in elderly
male patients with T2DM.</p>
<p class="art-para">The complex study including anthropometry of adipose
tissue in men suffering from T2DM would support the
evaluation of the prognosis of the disease.</p>

<p class="art-subhead" id="interests">Competing Interests</p>
<p class="art-para">The author has declared that no competing interests
exist. This research did not receive any specific grant from any
funding agency in the public, commercial or not-for-profit
sector. This article contains an original research and has not
been submitted/published earlier in any journal and is not
being considered for publication elsewhere. The paper was
approved by the corresponding author.</p>

<p class="art-subhead" id="approval">Ethical Approval</p>
<p class="art-para">An ethical approval was taken for this study from the
Ethics committee by Medical University-Plovdiv, Bulgaria.
Informed consents were taken from all patients involved in
the study.</p>

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