Anthropological Characteristic of the Distribution of Adipose Tissue in Bulgarian Females with Type 2 Diabetes Mellitus

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1 ORIGINAL ARTICLE, MEDICINE DOI: /folmed Anthropological Characteristic of the Distribution of Adipose Tissue in Bulgarian Females with Type 2 Diabetes Mellitus Atanas G. Baltadjiev 1, Stefka V. Vladeva 2, Dimitar B. Bahariev 1 1 Department of Anatomy, Histology and Embryology, Faculty of Medicine, Medical University of Plovdiv, Plovdiv, Bulgaria 2 Department of Endocrinology, Faculty of Medicine, St George University Hospital, Medical University of Plovdiv, Plovdiv, Bulgaria Correspondence: Atanas G. Baltadjiev, Department of Anatomy, Histology and Embryology, Faculty of Medicine, Medical University of Plovdiv, 15A Vassil Aprilov Blvd., 4000 Plovdiv, Bulgaria dr_atanas@abv.bg Tel.: Received: 21 Feb 2017 Accepted: 05 Dec 2017 Published Online: 02 Jan 2018 Published: 28 Sept 2018 Key words: type 2 diabetes mellitus, females, BMI, adipose tissue, skinfolds Citation: Baltadjiev AG, Vladeva SV, Bahariev DB. Anthropological characteristic of the distribution of adipose tissue in Bulgarian females with type 2 diabetes mellitus. Folia Med (Plovdiv) 2018;60(3): doi: /folmed Background: The complex study of adipose tissue in women with type 2 diabetes mellitus (T2DM) is of importance for the clinical course and prognosis of the disease. Aim: To study the distribution of adipose tissue in Bulgarian females with T2DM. Patients and methods: The study included 92 women with T2DM (age range years). The control group consisted of 40 age-matched women. Measurement parameters: height, weight, 9 skinfolds (sf) sftriceps, sfbiceps brachii, sfforearm, sfsubscapular, sfxrib, sfabdomen, sfsuprailiaca, sfthigh, and sfcalf; bioelectrical impedance analysis - % body fat tissue and visceral fat tissue. Calculated indexes: body mass index (BMI), the ratio sftrunk to sflimbs, the ratio skin folds upper half of body/skin folds lower half of body, fat mass and subcutaneous fat mass. Results: Statistically significant differences were found in the means of sftriceps, sfxrib, sfthigh, sfcalf, % body fat tissue, visceral fat tissue, and fat mass and subcutaneous fat mass between the diabetic and healthy women. The body composition of diabetic females aged years contained a larger adipose component than controls. Visceral adipose tissue which determines the body composition is a reliable indicator of the health risks in diabetic women. Conclusion: The pattern of subcutaneous adipose tissue distribution in diabetic females aged yrs was primarily in the upper torso region and less so in the limbs. In the controls adipose tissue is accumulated primarily in the limbs and in the lower part of the body. BACKGROUND Type 2 diabetes mellitus (T2DM) is a metabolic disease characterized by a failure to properly metabolize glucose due to a resistance to insulin. In recent years the disease has acquired many traits which could describe it as a social problem, and this is due to the rapidly rising number of individuals suffering from the condition. Globally, as of 2010, it was estimated that there were 285 million people with T2DM which is equivalent to about 6% of the world s adult population. 1 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, according to the International Diabetes Federation. It s about 10.3% of men and 9.6% of women aged 25 years and over. In Bulgaria around 8-9% of the population suffers from the disease. Most researchers are interested in the etiology, pathogenesis, clinical course and treatment of the disease. The anthropological status of diabetic patients enjoys little attention. Fat accumulation in the diabetic patients occurs primarily in two locations: in the abdomen (central, abdominal, visceral) and subcutaneously (peripheral). Common opinion holds that fat accumulation in the abdominal area is a risk factor for T2DM. 2-5 There has been very little research on the subcutaneous distribution of adipose tissue. The relevant literature offers little data on the complex deposition of adipose tissue in patients with T2DM. AIM The aim of this study was therefore to investigate the distribution of adipose tissue in year-old Bulgarian females with T2DM. Folia Medica I 2018 I Vol. 60 I No.3 411

2 A. Baltadjiev et al PATIENTS AND METHODS Ninety-two women with T2DM were included in the study. They were diagnosed by an endocrinologist and recruited from the Clinic of Endocrinology of St George University Hospital at the Medical University of Plovdiv, Bulgaria. The inclusion criteria were Bulgarian ethnicity, duration of the disease of no less than five years, compensated diabetes at the time of study, age range years (mean 52.87±0.56 SEM). The control group included 40 age-matched women (mean 51.33±0.93 SEM). The exclusion criteria were previous or existing metabolic, oncological or other disorder that could compromise the anthropological study. The anthropological methods we used included: Direct measurement parameters: Besides patient s height and 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. Bioelectrical Impedance analysis (BIA) - body fat tissue and visceral fat tissue percent (%) - was measured with a Body Composition Monitor Tanita. BC-532. Calculated indexes: body mass index (BMI); sftrunk/sflimbs ratio; skinfolds upper half of body/ skinfolds lower half of body ratio; fat mass and subcutaneous fat mass. STATISTICAL ANALYSIS Data were analyzed using SPSS v. 15 (SPSS Inc., Chicago, IL). Parametric statistical methods were relevant. Independent samples t test was used to compare the means of two independent anthropologic parameters in order to determine whether there was statistical evidence that the means were significantly different. The one-way analysis of variance (ANOVA) was used to determine whether there were any significant differences between the means of three or more independent parameters. P<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: ; moderate: ; strong: ; high: ; very high: >0.90. P<0.05 (two tailed) was considered statistically significant. RESULTS While in terms of age and height we found no difference between the mean values of the two studied groups, a significant difference was found between the means of weight - the value of diabetic females Table 1. Anthropological parameters of Bulgarian females with type 2 diabetes compared to healthy controls Type 2 diabetes mellitus Controls Parameters N Mean SEM SD N Mean SEM SD P Age (yrs) >0.05 Height (cm) >0.05 Weight (kg) <0.001 * sftriceps (mm) <0.05 * sfsubscapular (mm) >0.05 sfx rib (mm) <0.01 * sfsuprailiaca (mm) >0.05 sfabdomen (mm) >0.05 sfbiceps (mm) >0.05 sfforearm (mm) >0.05 sfthigh (mm) <0.001 * sfcalf (mm) <0.01 * sf: skinfold; *: statistically significant 412

3 Adipose Tissue in Type 2 Diabetes Mellitus Patients was higher than the controls (p<0.001) (Table 1). The thickness of sftriceps (brachii) of the diabetic females was significantly lower than the controls (p<0.05). The former, however was thicker in comparison to the sfbiceps and sfforearm of diabetic females. Also sftriceps was thinner than sfsubscapular, sfxrib and sfabdomen (ANOVA, p<0.001). The correlation analysis revealed a positive correlation (p<0.001) between the thicknesses of sftriceps and other skinfolds, as follows: the correlation was high to sfthigh (r=0.78) and sfcalf (r=0.73); strong - to sfbiceps, sfsubscapular, sfforearm, sfsuprailiaca, sfabdomen, and sfxrib (r= ) The thickness of sfsubscapular of the diabetic females was not different from the controls. The sf- Subscapular of diabetic women, however, was thicker in comparison to the sftriceps, sfsuprailiaca, sfbiceps, sfforearm and sfcalf of the same women (ANOVA, p<0.001). The correlation analysis revealed a positive correlation (p<0.001) between the thicknesses of sfsubscapular and other skinfolds as follows: strong correlation to sfxrib, sfbiceps, sfsuprailiaca, sftriceps, sfforearm, sfabdomen, and sfcalf (r= ); moderate correlation to sfthigh. The thickness of sfxrib of the diabetic females was significantly higher than that of the controls (p<0.01). The sfxrib of diabetic women was thicker than these of sftriceps, sfsuprailiaca, sfbiceps, sfforearm, and sfcalf of the same women; it was, however, thinner than sfabdomen (ANOVA, p<0.001). The correlation analysis revealed a positive correlation (p<0.001) between the thicknesses of sfxrib and other skinfolds, as follows: strong correlation to sfbiceps, sfabdomen, sfsuprailiaca, sfsubscapular, sfforearm, sftriceps, sfthigh, and sfcalf (r= ). There were not statistically significant differences in the thicknesses of sfsuprailiaca between diabetic females and healthy controls. SfSuprailiaca of diabetic women was thicker in comparison to the sfbiceps, and sfforearm of the same women, but it was thinner than sfsubscapular, sfxrib, and sfabdomen (ANOVA, p<0.001). The correlation analysis revealed a positive correlation between the thicknesses of sfsuprailiaca and other skinfolds, as follows: high correlation to sfabdomen in the same topographical area (r=0.76); strong correlation to sfxrib, sfsubscapular, sfforearm, sftriceps, sfbiceps, and sfcalf (r= ); moderate - to sfthigh. There were no statistically significant differences in the thicknesses of sfabdomen between diabetic females and healthy controls. SfAbdomen was the thickest skinfold among al studied skinfolds in diabetic women. It was thicker than the sfforearm, sfcalf, sftriceps, sfsuprailiaca, sfsubscapular, sfbiceps, sfthigh, and sfxrib (ANOVA, p<0.001). The correlation analysis revealed positive correlation between the thicknesses of sfabdomen and other skinfolds (p<0.001), as follows: high correlation to sfsuprailiaca (r=0.76); strong - to sfxrib, sfforearm, sfsubscapular, sftriceps, sfbiceps, and sfcalf (r= ); moderate - to sfthigh. The thickness of sfbiceps in the diabetic females was lower than the controls, but the difference did not reach statistical significance (p>0.05). SfBiceps was thicker than the sfforearm of diabetic women but it was thinner than the other skinfolds of the same women (ANOVA, p<0.001). The correlation analysis revealed positive correlations with the thicknesses of the studied skinfolds (p<0.001). The correlation was high with sfforearm (r=0.83) and sfcalf (r=0.74); strong with sfxrib, sftriceps, sfsubscapular, sfthigh, sfabdomen, and sfsuprailiaca (r= ). The thickness of sfthigh in the diabetic females was significantly lower than the controls (p<0.001). SfThigh was thicker than sfcalf, sfforearm, sfbiceps, but thinner than sfabdomen (ANOVA, p<0.001). The correlation analysis revealed positive correlation with the thicknesses of the other studied skinfolds (p<0.001). The correlation was high with sftriceps (r=0.78) and sfcalf (r=0.71); strong with sfbiceps, sfforearm, sfxrib (r= ); moderate with sfsubscapular, sfabdomen, and sfsuprailiaca. There was not any significant difference in the thicknesses of sfforearm between diabetic females and healthy controls. SfForearm was the thinnest among the other studied skinfolds (ANOVA, p<0.001). The correlation analysis revealed positive correlations of the sfforearm thickness with the other skinfolds (p<0.001). The correlation was high with sfbiceps (r=0.83) and sfcalf (r=0.71); strong with sfsuprailiaca, sfxrib, sfabdomen, sfsubscapular, sftriceps and sfthigh (r= ). The thickness of sfcalf in diabetic females was significantly lower than the healthy controls (p<0.01). It was thicker than sfforearm, and sfbiceps, but was thinner than sfsubscapular, sfxrib, sfabdomen and sfthigh (ANOVA, p<0.001). The correlation analysis revealed positive correlation of the sfcalf thickness with the other skinfolds (p<0.001). The correlation was high with sftriceps (r=0.73), sfbiceps (r=0.74), sfforearm and sfthigh (r=0.71); strong with sfsuprailiaca, sfxrib, sfabdomen and sfsubscapular (r= ). The accumulation of subcutaneous adipose tissue in patients with type 2 diabetes was higher in the torso than in the limbs. In contrast, the controls exhibited the 413

4 A. Baltadjiev et al opposite distribution. In women with type 2 diabetes 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 (Table 2). The BMI of the diabetic women was significantly known as central or visceral obesity, was more closely related to T2DM than the general obesity, as visceral fat was more metabolically active and produced more insulin resistance. 6-9 Similar data we observed in Bulgarian women aged with a diagnosis of T2DM. The values of the % fat Table 2. Anthropological indexes of Bulgarian females with type 2 diabetes compared to healthy controls Type 2 diabetes mellitus Controls sf Trunk/sf Limbs sf upper half of the body/sf lower half of the body sf: skinfold Table 3. Body composition of females with type 2 diabetes compared to healthy controls Type 2 diabetes mellitus Controls Parameters N Mean SEM SD N Mean SEM SD P BMI <0.001 * % body fat tissue <0.01 * Visceral fat tissue (kg) <0.001 * Fat mass (kg) <0.001 * Subcutaneous fat mass (kg) <0.05 * BMI: body mass index; *: statistically significant higher than that of the healthy controls (p<0.001) (Table 3). The body composition of diabetic females demonstrated a larger amount of adipose tissue than the controls. The values of the % body fat tissue of diabetic women were significantly higher than the controls (p<0.01). Approximately 40% from the body composition of the diabetic females was fat mass (FM) and the amounts of FM were also significantly higher than those of the controls (p<0.001). The values of the subcutaneous fat tissue in the controls, however, were higher compared to those of diabetic women (p<0.05). The data concerning the fat tissue components determine the body composition of diabetic patients as an important parameter regarding the prognosis of T2DM. The values of visceral fat tissue were significantly higher in the diabetic women, than in the controls (p<0.001). DISCUSSION It has been found that abdominal obesity, also mass, visceral adipose tissue and adipose tissue were statistically higher in women with T2DM than in the healthy controls. It was considered that this type of obesity increased the risk of pathological changes in other systems along with the progress of T2DM Attention should be paid to the distribution of subcutaneous adipose tissue in patients with T2DM. We found that in patients with T2DM the accumulation of subcutaneous adipose tissue was primarily in torso and less so in the limbs. Moreover, the accumulation of adipose tissue was predominantly in the upper body as compared to the lower, the so-called apple shaped pattern of distribution. These patients have a worse anthropological status, which would lead to a more severe clinical course of the disease In controls the deposition of adipose tissue was predominantly in the limbs and mainly in the lower part of the body, the so-called pear shaped pattern. 414

5 Adipose Tissue in Type 2 Diabetes Mellitus Patients As for the measurement of skinfold thickness, a positive correlation was established among them. 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. 17 In our investigation, the sfabdomen was the thickest, compared to the other studied skinfolds in patients with T2DM, but it did not differ significantly from the thickness of the corresponding skinfold in controls. Moreover, considerably greater thickness was measured in some skinfolds in the control group than in the corresponding skinfolds in patients with T2DM, as happened with sftriceps, sfthigh and sfcalf. These facts confirmed the greater importance of the accumulation of visceral than of subcutaneous fat for the course of the disease. 18 The levels of total weight and BMI were higher in diabetic women. They showed that women with T2DM were overweight and fattened compared to healthy controls, but these values had less importance to the course of the disease compared with the above-described parameters. 19 More original data about the anthropological status of Bulgarian patients with T2DM were published in our previous publications. 20 CONCLUSION The body composition of diabetic females aged years contained a larger common adipose component than the controls. The subcutaneous adipose tissue was accumulated mostly on the upper part of the torso. In the group of healthy women (controls), the subcutaneous adipose tissue was accumulated mostly in the peripheral part of the body (arms, thighs and lower legs). The bioelectrical impedance analysis of the body composition demonstrated that the visceral adipose tissue in females patients suffering from T2DM was significant more expressed than the healthy controls. It applied to visceral adipose tissue which determined the body composition in persons with T2DM as unfavorable to the progress of the disease. The complex study including anthropometry of adipose tissue in women with T2DM would support the evaluation of the clinical course, treatment, and prognosis of the disease. This study is a part from the larger survey including female patients years as well as male patients from the both age groups in Bulgaria. The anthropological parameters provided 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 suffering from T2DM. REFERENCES 1. Melmed S, Polonsky KS, Larsen PR, et al. Chapter 1: Principles of Endocrinology. In: Melmed S, Polonsky KS, Larsen PR, Kronenberg HM, editors. Williams Textbook of Endocrinology, 12th ed. Philadelphia: Elsevier/Saunders; p Folsom AR, Kushi LH, Anderson KE, et al. Associations of general and abdominal obesity with multiple health outcomes in older women: the Iowa Women s Health Study. Arch Intern Med 2000;160(14): Janssen I, Katzmarzyk PT, Ross R. Waist circumference and not body mass index explains obesity-related health risk. Am J Clin Nutr 2004;79(3): Meisinger C, Döring A, Thorand B, et al. Body fat distribution and risk of type 2 diabetes in the general population: are there differences between men and women? The MONICA/KORA Augsburg cohort study. Am J Clin Nutr 2006;84(3): Snijder MB, van Dam RM, Visser M, et al. What aspects of body fat are particularly hazardous and how do we measure them? Int J Epidemiol 2006;35(1): Hauner H. Managing type 2 diabetes mellitus in patients with obesity. Treat Endocrinol 2004;3(4): Sam S, Haffner S, Davidson MH, et al. Relationship of abdominal visceral and subcutaneous adipose tissue with lipoprotein particle number and size in type 2 diabetes. Diabetes 2008;57(8): Shrestha OK, Shrestha GL. Visceral fat versus subcutaneous fat: comparison of their association with type 2 diabetes mellitus. Journal of Chitwan Medical College 2014;4(2): Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr 2000;71(4): Kim TH, Lee SS, Yoo JH, et al. The relationship between the regional abdominal adipose tissue distribution and the serum uric acid levels in people with type 2 diabetes mellitus. Diabetol Metab Syndr 2012;4(1): Kim SR, Yoo JH, Song HC, et al. Relationship of visceral and subcutaneous adiposity with renal function in people with type 2 diabetes mellitus. Nephrol Dial Transplant 2011;26(11):

6 A. Baltadjiev et al 12. Jung CH, Kim BY, Kim KJ, et al. Contribution of subcutaneous abdominal fat on ultrasonography to carotid atherosclerosis in patients with type 2 diabetes mellitus. Cardiovasc Diabetol 2014;13: Heshka S, Ruggiero A, Bray GA, et al. Altered body composition in type 2 diabetes mellitus. Int J Obes 2008;32(5): Tafeit E, Möller R, Pieber TR, et al. Differences of subcutaneous adipose tissue topography in type-2 diabetic (NIDDM) women and healthy controls. Am J Phys Anthropol 2000;113(3): Livingston EH. Lower body subcutaneous fat accumulation and diabetes mellitus risk. Surg Obes Relat Dis 2006;2(3): Patel P, Abate N. Body fat distribution and insulin resistance. Nutrients 2013;5(6): Ristic P, Bokonjic D, Zivkovic V, et al. Subcutaneous adipose tissue measurements and better metabolic prediction. Central European Journal of Medicine 2013;8(2): Jørgensen ME, Borch-Johnsen K, Stolk R, et al. Fat distribution and glucose intolerance among Greenland Inuit. Diabetes Care 2013;36(10): Shirafkan A, Marjani A. Prevalence of obesity among type 2 diabetes mellitus in Gorgan (South East of Caspian Sea), Iran. World Applied Sciences Journal 2011;14(9): Baltadjiev A. [Morpho-anthropological characteristics of patients with type 2 diabetes mellitus] [dissertation]. Plovdiv: MU-Plovdiv; 2010 (Bulgarian). Антропологические характеристики распределения жировой ткани среди женщин с сахарным диабетом 2-ого типа из Болгарии Атанас Г. Балтаджиев 1, Стефка В. Владева 2, Димитр Б. Бахариев 1 1 Кафедра анатомии, гистологии и эмбриологии, Факультет медицины, Медицинский университет- Пловдив, Пловдив, Болгария 2 Кафедра эндокринологии, Факультет медицины, Университетская больница Св. Георги, Пловдив, Болгария Адрес для корреспонденции: Атанас Г. Балтаджиев Кафедра анатомии, гистологии и эмбриологии, Факультет медицины, Медицинский университет- Пловдив, бул. Васил Априлов 15 А, 4000, Пловдив, Болгария dr_atanas@abv.bg Тел.: Дата получения: 21 февраля 2017 Дата приемки: 05 декабря 2017 Дата онлайн публикации: 02 января 2018 Дата публикации: 28 сентября 2018 Ключевые слова: сахарный диабет 2-ого типа, женщины, ИТМ, жировая ткань, кожные складки Образец цитирования: Baltadjiev AG, Vladeva SV, Bahariev DB. Anthropological characteristic of the distribution of adipose tissue in Bulgarian females with type 2 diabetes mellitus. Folia Med (Plovdiv) 2018;60(3): doi: /folmed Введение: Комплексное исследование жировой ткани среди женщин с сахарным диабетом 2-ого типа (СД2) играет важную роль в отношении клинического протекания и прогноза заболевания. Цель: Исследовать распределение жировой ткани среди женщин с СД2 из Болгарии. Пациенты и методы: В исследовании приняло участие 92 женщины с СД2 (возрастной диапазон лет). Контрольная группа состояла из 40 женщин, отобранных в соответствии с возрастным диапазоном. Измеряемые параметры: высота, вес, 9 кожных складок (КС) - КС трицепса, КС бицепса, КС предплечья, субскапулярные КС, КС над X-ым ребром, надвздошные КС, КС бедра, икроножные КС; биоэлектрический анализ импеданса (БАИ) - % телесной жировой ткани и висцеральной жировой ткани. Расчётные показатели - индекс массы тела (ИМТ), соотношение КС корпуса и КС конечностей, соотношение КС верхней части тела и КС нижней половины тела, жировой массы и подкожного жира. Результаты: Статистически значимые различия были установлены при средних значениях КС трицепса, КС Х-ого ребра, КС бедра, икроножных КС, % жировой ткани в организме, висцерального жира и подкожного жира между здоровыми женщинами и женщинами, страдающими диабетом. Состав тела у женщин, страдающих диабетом в возрасте лет, содержит большее количество жирового компонента, по сравнению с контрольной группой. Висцеральный жир, который определяет состав тела, является надёжным показателем риска для здоровья женщин, страдающих диабетом. Выводы: Структура распределения подкожной жировой ткани у женщин, страдающих диабетом в возрасте лет, была установлена главным образом в верхней части тела и в меньшей степени в конечностях. В контрольной группе жировая ткань накапливалась главным образом в конечностях и в нижней части тела. 416