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Vascular OnlineFirst, published on September 22, 2014 as doi:10.1177/1708538114552012
Original Article
Investigation of relation between visceral and subcutaneous abdominal fat volumes and calcified aortic plaques via multislice computed tomography
Vascular 0(0) 1–7 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1708538114552012 vas.sagepub.com
Duran Efe1, Fatih Aygu¨n2, Tu¨rker Acar1, Melda Yildiz1 and Kazım Gemici3
Abstract Objective: The present study investigated effect of subcutaneous fat volume and abdominal visceral fat volume on aortic atherosclerosis via multislice computed tomography. Materials and methods: The present study comprised 424 subjects who underwent non-contrast-enhanced abdominal CT in our clinic between June 2012 and June 2013. Using dedicated software visceral fat volume was calculated for each individual and then subcutaneous fat volume was calculated by subtracting visceral fat volume from total fat volume. By dividing visceral fat volume/subcutaneous fat volume participants were assigned to three groups according to their mean visceral fat volume/subcutaneous fat volume: Group 1 consisted of subjects with visceral fat volume/subcutaneous fat volume lower than 0.48 (Group 1 < 0.48); Group 2 consisted of subjects with visceral fat volume/subcutaneous fat volume equal to or higher than 0.48 and lower than 0.69 (0.48 Group 2 < 0.69); and Group 3 consisted of subjects with visceral fat volume/subcutaneous fat volume equal to or higher than 0.69 (Group 3 0.69). Results: The mean abdominal aortic calcium scores according to Agatston scoring (au) were 136.8 418.7 au in Group 1, 179.9 463 au in Group 2 and 212.2 486.9 in Group 3, respectively. Conclusions: We have demonstrated a significant correlation between visceral fat volume and abdominal aorta atherosclerosis, while there was absence of significant correlation between subcutaneous fat volume and abdominal atherosclerosis.
Keywords Multislice computed tomography, visceral adipose tissue, subcutaneous adipose tissue, arteriosclerosis, calcification
Introduction Prevalence of overweight and obesity is gradually increasing in the developed countries.1–3 Obesity is associated with atherosclerotic plaques, cardiovascular diseases and metabolic risk factors.4–7 Although body mass index (BMI) is a useful indicator for overall adiposity, various adipose components in the body might be associated with various metabolic risks.8 Waist circumference (WC) is a function of subcutaneous and visceral adipose tissues and is not a precise measurement for abdominal adiposity.9 Abdominal adiposity could be more atherogenic than whole body adiposity. Previous studies have determined strong correlation between central obesity and coronary and abdominal aortic calcium plaques.10,11
The present study aimed to investigate effect of subcutaneous fat volume (SFV) and abdominal visceral fat volume (VFV) on aortic atherosclerosis (AA) via multislice CT (MSCT).
1 Department of Radiology, Faculty of Medicine, Mevlana University, Konya, Turkey 2 Bas¸kent University, Konya Medical and Research Center, Department of Cardiovascular Surgery, Turkey 3 Department of General Surgery, Faculty of Medicine, Mevlana University, Konya, Turkey
Corresponding author: Fatih Aygu¨n, Hoca cihan mahallesi Saray Caddesi No:1,42000 Selc¸ukluKonya/Tu¨rkiye. Email: [email protected]
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Materials and methods Clinical characteristics of patients The present study comprised 424 subjects that underwent non-contrast-enhanced abdominal computed tomography (CT) in our clinic between June 2012 and June 2013. The subjects had no primary hyperparathyroidism, renal tubular acidosis or similar metabolic diseases. Data were collected retrospectively and approval of ethical committee was obtained. All subjects were investigated in terms of smoking, hypertension, diabetes mellitus and hyperlipidemia. Height (Human scale, NAN TARTI Inc. Turkey) and weight (TANITA Body Composition Analyzer, TANITA Corporation, Japan) of the study participants were measured before CT, and body mass indexes (BMI) were calculated. Subjects with BMI less than 25 kilogram (kg)/square meter (m2) (BMI < 25 kg/m2) were considered normal weight; subjects with BMI between 25 kg/m2 and 30 kg/m2 (25 kg/ m2 BMI < 30 kg/m2) were considered overweight; and subjects with BMI 30 kg/m2 and over (30 kg/m2 BMI) were considered obese.
Figure 1. Axial CT section shows the measurement of abdominal total adipose tissue volume.
Abdominal MSCT image reconstruction All subjects underwent non-contrast-enhanced abdominal CT (Somatom Sensation 64, Siemens, Forchheim, Germany) at 0.6 millimeter (mm) sections beginning from subdiaphragmatic level extending towards the level of symphysis pubis. The scan parameters were 64 0.625 mm collimation, tube voltage 100–120 millivolt (mV), and effective milliamper (mA) 350–780 mA. Total fat volume (TFV) and VFV measurements were done using software (Syngo volume analysis, Leonardo, Siemens) and axial single-section at the level of intervertebral disc between 4th and 5th lumbar vertebra (L4–L5), which has been defined in the previous studies. Abdominal fat volume (Figure 1) and VFV (Figure 2) were measured as cubic centimeter (cm3) using Manuel Region of interest (ROI) drawings.12 Fat appears as low-density areas on CT images and it was identified as the areas of attenuation values of 195 to 45 Hounsfield units according to standardized protocol.13
Abdominal aortic calcium scoring Abdominal aortic calcium scores (AaCs) between celiac trunk and iliac bifurcation were measured as Agatston units (au) (Figure 3). Calcium scoring was evaluated using the software (Syngo CaScore, Siemens, Forchheim, Germany, Agatston scoring method) that already existed in the device.14
Figure 2. Axial CT section shows the measurement of abdominal visceral adipose tissue volume.
Groups The study comprised a total of 424 subjects. All study participants underwent TFV and VFV measurement after abdominal CT. These measurements were done by the same radiologist. SFV was calculated by subtracting VFV from TFV.15 Study participants were assigned to three groups according to their mean VFV/SFV: Group 1 consisted of subjects with VFV/SFV lower than 0.48 (Group 1 < 0.48); Group 2 consisted of subjects with VFV/SFV equal to or higher than 0.48 and lower than 0.69 (0.48 Group 2 < 0.69); and Group 3 consisted of subjects with VFV/SFV equal to or higher than 0.69 (Group 3 0.69).
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Statistical analysis Statistical analyses were done using SPSS program (SPSS Inc., Chicago, IL, USA). Statistical significance of non-parametric data between the groups was analyzed by Pearson Chi-square analysis. Parametric data were represented as minimum, maximum, mean standard deviation, whereas statistical significance of parametric data between the groups was analyzed by one-way ANOVA test. From which group the difference arouse as the result of variance
analysis was assessed by post hoc analysis (multiple comparison was performed using Games-Howell). The result was considered to be statistically significant if p value was smaller than 0.05 (p < 0.05) (Table 1).
Results Subject characteristics Age distribution of all participants was minimum (min) 19 years (y) and maximum (max) 87 years (mean standard deviation 42.6 13.8 y). Of these subjects, 271 (63.9%) were male and 153 (36.1%) were female. There were 92 (21.7%) subjects with hypertension, 158 (37.3%) smokers and 52 (12.3%) subjects with diabetes mellitus. The number of subjects with dyslipidemia was 80 (18.9%). According to the BMI, there were 126 (29.7%) normal-weight subjects, 155 (36.6%) overweight subjects and 143 (33.7%) obese subjects. Among participants, aortic calcium score (AaCs) was min 0 au and max 2201 au (mean standard deviation 230 516.7), whereas VFV/SFV was found min 0.18 and max 3.4.
Groups characteristics
Figure 3. Coronal CT section shows widespread calcified plaques in the abdominal aorta.
Group 1 consisted of subjects with VFV/SFV lower than 0.48 (Group 1 < 0.48); Group 2 consisted of subjects with VFV/SFV equal to or higher than 0.48 and lower than 0.69 (0.48 Group 2 < 0.69); and Group 3
Table 1. Data of the groups and results of statistics are demonstrated.
Age (years) ( SD) Gender (male) Smoking BMI normal overweight obes Diabetes mellitus (type 2) Dislipidemia Hypertension Subcutan faty volume (SFV) (cm3) Visseral faty volume (VFV) (cm3) VFV/SFV ratio Abdominal aortic calcium scoring (AaCs) (au)
Group 1 (n ¼ 138)
Group 2 (n ¼ 141)
Group 3 (n ¼ 145)
42.4 13.2 51 (% 37) 57 (% 41.3) 36 (% 26.1) 66 (% 47.8) 36 (% 26.1) 5 (% 3.6) 18 (% 13) 31 (% 22.5) 371.2 132.4 136 48.9 0.37 0.07 136.8 418.7 C
40.1 13.3 93 (% 66) 50 (% 35.5) 42 (% 29.8) 47 (% 33.3) 52 (% 36.9) 15 (% 10.6) 26 (% 18.4) 19 (% 13.5) 290.5 121.6 166.7 66.1 0.58 0.06 179.9 463B
45.3 14.4 127 (% 87.6) 51 (% 35.2) 48 (% 33.1) 42 (% 29) 55 (% 37.9) 32 (% 22.1) 36 (% 24.8) 42 (% 29) 201.5 90.1 188 139.7 0.96 0.40 212.2 486.9 A
BMI: body mass ındex; SD: standard deviation. a p Value was presented as a result of ONE-WAY ANOVA test. b p Value was presented as a result of Pearson Chi-square test. Among the same row averages carrying different capital letters are statistically important (p < 0.01). Among the same row averages carrying different lower case letters are statistically important (p < 0.05).
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p Value 0.01a 0b 0.489b 0.068b
0b 0.040b 0.006b 0a 0a 0a 0a
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consisted of subjects with VFV/SFV equal to or higher than 0.69 (Group 3 0.69). In males of Group 1, mean VFV/SFV was 0.39 0.08, age was 39.2 11.6 y and mean abdominal aortic calcium score according to agatston scoring was 126.4 489.1 au. There were 18 (35.3%) obese subjects, 25 (49%) smokers, 8 (15.7%) subjects with hypertension, 3 (5.9%) subjects with dyslipidemia and 5 (% 9.8) subjects with diabetes mellitus. In females of Group 1, it was observed that mean VFV/SFV was 0.36 0.06, mean age was 44.2 13.8 y and mean abdominal aortic calcium score according to agatston scoring was 142.9 374.2 au. There were 18 (20.7%) obese subjects, 32 (36.8%) smokers, 23 (26.4%) subjects with hypertension, 15 (17.2%) subjects with dyslipidemia and no subject with diabetes mellitus. In males of Group 2, it was observed that mean VFV/SFV was 0.59 0.06, mean age was 38 10.5 y and mean abdominal aortic calcium score according to agatston scoring was 164.8 439.9 au. There were 34 (36.6%) obese subjects, 34 (36.6%) smokers, 8 (8.6%) subjects with hypertension, 14 (15.1%) subjects with dyslipidemia and 8 (8.6%) subjects with diabetes mellitus. In females of Group 2, it was determined that mean VFV/SFV was 0.55 0.05 and mean abdominal aortic calcium score according to agatston scoring was 209 508.2 au. There were 18 (37.5%) obese subjects, 16 (33.3%) smokers, 11 (22.9%) subjects with hypertension, 12 (25%) subjects with dyslipidemia and 7 (14.6%) subjects with diabetes mellitus. In males of Group 3, the mean VFV/SFV was 0.93 0.28 and mean abdominal aortic calcium score
according to agatston scoring was 369 644.6 au. There were 50 (39.4%) obese subjects, 48 (37.8%) smokers, 33 (26%) subjects with hypertension, 36 (28.3%) subjects with dyslipidemia and 29 (22.8%) subjects with diabetes mellitus. In females of Group 3, it was determined that mean VFV/SFV was 1.1 0.87 and mean abdominal aortic calcium score according to agatston scoring was 356.2 363.1 au. There were 5 (27.8%) obese subjects, 3 (16.7%) smokers, 9 (50%) subjects with hypertension, no subject with dyslipidemia and 3 (16.7%) subjects with diabetes mellitus. Among all participants, SFV was 247.2 114.8 cm3, VFV was 160.5 62.1 cm3 and AaCs was 253.3 562.3 au in male subjects, whereas SFV was 355.8 139.7 cm3, VFV was 170.2 137.9 cm3 and AaCs was 188.7 422.5 au in female subjects. Whilst mean AaCs was statistically significantly higher in males versus females, mean SFV was statistically significantly higher in females versus males. You can see mean AaCS according to age in male patient in Figure 4(a) and in female patient in Figure 4(b). In the present study, the number of hypertensive patients was determined to be the highest in Group 3. The difference between the groups in terms of hypertension was statistically significant (p < 0.05) (p ¼ 0.006). Participants with dyslipidemia were more prevalent in Group 3. Statistically significant difference was determined between the groups in terms of dyslipidemia (p < 0.05) (p ¼ 0.04). Analysis concerning Type 2 diabetes mellitus revealed that number of type 2 diabetic patients was higher in Group 3 as compared to the other groups. The difference between the groups in terms of Type 2 diabetes was found to be statistically
Figure 4. (a) Mean AaCS according to age in male patients; (b) Mean AaCS according to age in female patients. AaCs: Abdominal Aortic Calcium Scoring; au: Agatston units.
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significant (p < 0.05) (p ¼ 0). The mean VFV was found low in the subjects with low mean AaCs (Group 1), whereas mean VFV was found high in the subjects with high mean AaCs (Group 3) and the difference was statistically significant (p < 0.01) (p ¼ 0). Data of the groups and results of statistics are demonstrated in Table 1.
Discussion Abdominal SFV and VFV were measured via MSCT and their relation with abdominal aortic calcium score, which is considered as atherosclerosis marker, was investigated in the subjects who participated in the present study. Statistically significant difference was determined between Group 3 and Group 2 (p < 0.05) (p ¼ 0.01) and between Group 3 and Group 1 (p < 0.01) (p ¼ 0.001) in terms of mean AaCs; whereas the difference between Group 2 and Group 1 was found to be statistically insignificant (p > 0.05) (p ¼ 0.69). It was found that the difference between the groups in terms of mean SFV was statistically significant, but relation with AaCs was statistically insignificant. Statistically significant difference was determined between Group 1 and Group 2 (p < 0.01) (p ¼ 0) and between Group 1 and Group 3 (p < 0.01) (p ¼ 0) in terms of mean VFV; whereas the difference between Group 2 and group 3 was found to be statistically insignificant (p > 0.05) (p ¼ 0.22). In the literature many studies exist regarding fat content. In these studies VFV and SFV was measured using CT. The comparison of visceral adipose tissue and subcutaneous adipose tissue has revealed that cardiometabolic risk factors have been found to be more associated with VFV.16–18 Rosenquist et al.19 investigated the interaction between cardiometabolic risks and visceral fat and subcutaneous fat tissue. According to the aforementioned study, they found that the increase in the VFV and SFV will intensify the cardiometabolic risks. Many studies found that increase in the amount of visceral adipose tissue is associated with dyslipidemia, type 2 diabetes, systemic inflammation and hypertension.20–25 Some studies focused on human adipose tissue vascularity and angiogenic properties.26,27 Several studies demonstrated inverse correlation between systemic insulin resistance indicators and average adipose tissue volume with the evaluation of fat biopsies.28,29 Recent studies regarding visceral and subcutaneous adipose tissue showed that BMI and morbid obesity decreased the angiogenic potential of adipose tissue.15–27 It is also stated in the literature that adipose tissue may increase cardiometabolic risks via inflammation and macrophage accumulation.31–32
Alexandersen et al.33 determined correlation between aortic calcified plaque measurements on lateral x-ray and truncal fat mass measured on x-ray absorptiometry in 168 male patients that had serious abdominal aortic calcified plaque.33 Whereas only serious abdominal aortic calcified plaque can be measured on x-ray, MSCT could have measured millimetric calcified plaques in the present study. The mean VFV was found low in the subjects with low mean AaCs (Group 1), whereas mean VFV was found high in the subjects with high mean AaCs (Group 3) and the difference was statistically significant (p < 0.01) (p ¼ 0). Anthropometric measurements may be unable to differentiate between VFV and SFV. Results of correlation between anthropometric measurements and subcutaneous and VFVs show difference in the studies carried out in different ethnic groups.34,35 No correlation was found between BMI and VFV in the South Asian populations.36 In the present study, no correlation was determined between BMI and VFV and between BMI and SFV. In the literature, there are different results concerning correlation between BMI and SFV and VFV. We believe that abdominal fat distribution should be measured by a direct and precise method such as MSCT and magnetic resonance imaging (MRI) for potential cardiometabolic results.
Conclusion Based on the results of present study, the first finding that would contribute to the literature is the notable increase observed in the risk of aortic atherosclerosis in Group 3. The second finding is the absence of significant correlation found between SFV and abdominal atherosclerosis. The last finding is statistically significant relation found between abdominal aortic atherosclerosis and abdominal VFV. We believe that determination of visceral and SFVs during routine abdominal MSCT scanning and informing the subjects in risky groups about cardiometabolic diseases would be beneficial.
Study limitations In the present study, the amounts of abdominal visceral fat tissue and subcutaneous fat tissue have been measured in a single section and as volume. Total amount of abdominal fat has not been studied in volumes. Furthermore, study participants were all from the same geographical region and were all Caucasians; thus, they do not represent other ethnic groups or different geographical regions. In some races such as Japanese Americans and Southeastern Asians, expected VFVs are higher as compared to BMIs.37 Therefore, larger epidemiological studies that would be performed
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in different geographical regions are needed to confirm the results of present study. Acknowledgments We thank Assoc. Prof. Ismail Keskin, PhD (Selc¸uk University, Zootechnics Division, Department of Biometry and Genetics, Konya, Turkey), for his contributions to the evaluation of results and statistical analysis.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Conflict of Interest None declared.
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Vascular OnlineFirst, published on September 22, 2014 as doi:10.1177/1708538114552012
Original Article
Investigation of relation between visceral and subcutaneous abdominal fat volumes and calcified aortic plaques via multislice computed tomography
Vascular 0(0) 1–7 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1708538114552012 vas.sagepub.com
Duran Efe1, Fatih Aygu¨n2, Tu¨rker Acar1, Melda Yildiz1 and Kazım Gemici3
Abstract Objective: The present study investigated effect of subcutaneous fat volume and abdominal visceral fat volume on aortic atherosclerosis via multislice computed tomography. Materials and methods: The present study comprised 424 subjects who underwent non-contrast-enhanced abdominal CT in our clinic between June 2012 and June 2013. Using dedicated software visceral fat volume was calculated for each individual and then subcutaneous fat volume was calculated by subtracting visceral fat volume from total fat volume. By dividing visceral fat volume/subcutaneous fat volume participants were assigned to three groups according to their mean visceral fat volume/subcutaneous fat volume: Group 1 consisted of subjects with visceral fat volume/subcutaneous fat volume lower than 0.48 (Group 1 < 0.48); Group 2 consisted of subjects with visceral fat volume/subcutaneous fat volume equal to or higher than 0.48 and lower than 0.69 (0.48 Group 2 < 0.69); and Group 3 consisted of subjects with visceral fat volume/subcutaneous fat volume equal to or higher than 0.69 (Group 3 0.69). Results: The mean abdominal aortic calcium scores according to Agatston scoring (au) were 136.8 418.7 au in Group 1, 179.9 463 au in Group 2 and 212.2 486.9 in Group 3, respectively. Conclusions: We have demonstrated a significant correlation between visceral fat volume and abdominal aorta atherosclerosis, while there was absence of significant correlation between subcutaneous fat volume and abdominal atherosclerosis.
Keywords Multislice computed tomography, visceral adipose tissue, subcutaneous adipose tissue, arteriosclerosis, calcification
Introduction Prevalence of overweight and obesity is gradually increasing in the developed countries.1–3 Obesity is associated with atherosclerotic plaques, cardiovascular diseases and metabolic risk factors.4–7 Although body mass index (BMI) is a useful indicator for overall adiposity, various adipose components in the body might be associated with various metabolic risks.8 Waist circumference (WC) is a function of subcutaneous and visceral adipose tissues and is not a precise measurement for abdominal adiposity.9 Abdominal adiposity could be more atherogenic than whole body adiposity. Previous studies have determined strong correlation between central obesity and coronary and abdominal aortic calcium plaques.10,11
The present study aimed to investigate effect of subcutaneous fat volume (SFV) and abdominal visceral fat volume (VFV) on aortic atherosclerosis (AA) via multislice CT (MSCT).
1 Department of Radiology, Faculty of Medicine, Mevlana University, Konya, Turkey 2 Bas¸kent University, Konya Medical and Research Center, Department of Cardiovascular Surgery, Turkey 3 Department of General Surgery, Faculty of Medicine, Mevlana University, Konya, Turkey
Corresponding author: Fatih Aygu¨n, Hoca cihan mahallesi Saray Caddesi No:1,42000 Selc¸ukluKonya/Tu¨rkiye. Email: [email protected]
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Materials and methods Clinical characteristics of patients The present study comprised 424 subjects that underwent non-contrast-enhanced abdominal computed tomography (CT) in our clinic between June 2012 and June 2013. The subjects had no primary hyperparathyroidism, renal tubular acidosis or similar metabolic diseases. Data were collected retrospectively and approval of ethical committee was obtained. All subjects were investigated in terms of smoking, hypertension, diabetes mellitus and hyperlipidemia. Height (Human scale, NAN TARTI Inc. Turkey) and weight (TANITA Body Composition Analyzer, TANITA Corporation, Japan) of the study participants were measured before CT, and body mass indexes (BMI) were calculated. Subjects with BMI less than 25 kilogram (kg)/square meter (m2) (BMI < 25 kg/m2) were considered normal weight; subjects with BMI between 25 kg/m2 and 30 kg/m2 (25 kg/ m2 BMI < 30 kg/m2) were considered overweight; and subjects with BMI 30 kg/m2 and over (30 kg/m2 BMI) were considered obese.
Figure 1. Axial CT section shows the measurement of abdominal total adipose tissue volume.
Abdominal MSCT image reconstruction All subjects underwent non-contrast-enhanced abdominal CT (Somatom Sensation 64, Siemens, Forchheim, Germany) at 0.6 millimeter (mm) sections beginning from subdiaphragmatic level extending towards the level of symphysis pubis. The scan parameters were 64 0.625 mm collimation, tube voltage 100–120 millivolt (mV), and effective milliamper (mA) 350–780 mA. Total fat volume (TFV) and VFV measurements were done using software (Syngo volume analysis, Leonardo, Siemens) and axial single-section at the level of intervertebral disc between 4th and 5th lumbar vertebra (L4–L5), which has been defined in the previous studies. Abdominal fat volume (Figure 1) and VFV (Figure 2) were measured as cubic centimeter (cm3) using Manuel Region of interest (ROI) drawings.12 Fat appears as low-density areas on CT images and it was identified as the areas of attenuation values of 195 to 45 Hounsfield units according to standardized protocol.13
Abdominal aortic calcium scoring Abdominal aortic calcium scores (AaCs) between celiac trunk and iliac bifurcation were measured as Agatston units (au) (Figure 3). Calcium scoring was evaluated using the software (Syngo CaScore, Siemens, Forchheim, Germany, Agatston scoring method) that already existed in the device.14
Figure 2. Axial CT section shows the measurement of abdominal visceral adipose tissue volume.
Groups The study comprised a total of 424 subjects. All study participants underwent TFV and VFV measurement after abdominal CT. These measurements were done by the same radiologist. SFV was calculated by subtracting VFV from TFV.15 Study participants were assigned to three groups according to their mean VFV/SFV: Group 1 consisted of subjects with VFV/SFV lower than 0.48 (Group 1 < 0.48); Group 2 consisted of subjects with VFV/SFV equal to or higher than 0.48 and lower than 0.69 (0.48 Group 2 < 0.69); and Group 3 consisted of subjects with VFV/SFV equal to or higher than 0.69 (Group 3 0.69).
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Statistical analysis Statistical analyses were done using SPSS program (SPSS Inc., Chicago, IL, USA). Statistical significance of non-parametric data between the groups was analyzed by Pearson Chi-square analysis. Parametric data were represented as minimum, maximum, mean standard deviation, whereas statistical significance of parametric data between the groups was analyzed by one-way ANOVA test. From which group the difference arouse as the result of variance
analysis was assessed by post hoc analysis (multiple comparison was performed using Games-Howell). The result was considered to be statistically significant if p value was smaller than 0.05 (p < 0.05) (Table 1).
Results Subject characteristics Age distribution of all participants was minimum (min) 19 years (y) and maximum (max) 87 years (mean standard deviation 42.6 13.8 y). Of these subjects, 271 (63.9%) were male and 153 (36.1%) were female. There were 92 (21.7%) subjects with hypertension, 158 (37.3%) smokers and 52 (12.3%) subjects with diabetes mellitus. The number of subjects with dyslipidemia was 80 (18.9%). According to the BMI, there were 126 (29.7%) normal-weight subjects, 155 (36.6%) overweight subjects and 143 (33.7%) obese subjects. Among participants, aortic calcium score (AaCs) was min 0 au and max 2201 au (mean standard deviation 230 516.7), whereas VFV/SFV was found min 0.18 and max 3.4.
Groups characteristics
Figure 3. Coronal CT section shows widespread calcified plaques in the abdominal aorta.
Group 1 consisted of subjects with VFV/SFV lower than 0.48 (Group 1 < 0.48); Group 2 consisted of subjects with VFV/SFV equal to or higher than 0.48 and lower than 0.69 (0.48 Group 2 < 0.69); and Group 3
Table 1. Data of the groups and results of statistics are demonstrated.
Age (years) ( SD) Gender (male) Smoking BMI normal overweight obes Diabetes mellitus (type 2) Dislipidemia Hypertension Subcutan faty volume (SFV) (cm3) Visseral faty volume (VFV) (cm3) VFV/SFV ratio Abdominal aortic calcium scoring (AaCs) (au)
Group 1 (n ¼ 138)
Group 2 (n ¼ 141)
Group 3 (n ¼ 145)
42.4 13.2 51 (% 37) 57 (% 41.3) 36 (% 26.1) 66 (% 47.8) 36 (% 26.1) 5 (% 3.6) 18 (% 13) 31 (% 22.5) 371.2 132.4 136 48.9 0.37 0.07 136.8 418.7 C
40.1 13.3 93 (% 66) 50 (% 35.5) 42 (% 29.8) 47 (% 33.3) 52 (% 36.9) 15 (% 10.6) 26 (% 18.4) 19 (% 13.5) 290.5 121.6 166.7 66.1 0.58 0.06 179.9 463B
45.3 14.4 127 (% 87.6) 51 (% 35.2) 48 (% 33.1) 42 (% 29) 55 (% 37.9) 32 (% 22.1) 36 (% 24.8) 42 (% 29) 201.5 90.1 188 139.7 0.96 0.40 212.2 486.9 A
BMI: body mass ındex; SD: standard deviation. a p Value was presented as a result of ONE-WAY ANOVA test. b p Value was presented as a result of Pearson Chi-square test. Among the same row averages carrying different capital letters are statistically important (p < 0.01). Among the same row averages carrying different lower case letters are statistically important (p < 0.05).
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p Value 0.01a 0b 0.489b 0.068b
0b 0.040b 0.006b 0a 0a 0a 0a
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consisted of subjects with VFV/SFV equal to or higher than 0.69 (Group 3 0.69). In males of Group 1, mean VFV/SFV was 0.39 0.08, age was 39.2 11.6 y and mean abdominal aortic calcium score according to agatston scoring was 126.4 489.1 au. There were 18 (35.3%) obese subjects, 25 (49%) smokers, 8 (15.7%) subjects with hypertension, 3 (5.9%) subjects with dyslipidemia and 5 (% 9.8) subjects with diabetes mellitus. In females of Group 1, it was observed that mean VFV/SFV was 0.36 0.06, mean age was 44.2 13.8 y and mean abdominal aortic calcium score according to agatston scoring was 142.9 374.2 au. There were 18 (20.7%) obese subjects, 32 (36.8%) smokers, 23 (26.4%) subjects with hypertension, 15 (17.2%) subjects with dyslipidemia and no subject with diabetes mellitus. In males of Group 2, it was observed that mean VFV/SFV was 0.59 0.06, mean age was 38 10.5 y and mean abdominal aortic calcium score according to agatston scoring was 164.8 439.9 au. There were 34 (36.6%) obese subjects, 34 (36.6%) smokers, 8 (8.6%) subjects with hypertension, 14 (15.1%) subjects with dyslipidemia and 8 (8.6%) subjects with diabetes mellitus. In females of Group 2, it was determined that mean VFV/SFV was 0.55 0.05 and mean abdominal aortic calcium score according to agatston scoring was 209 508.2 au. There were 18 (37.5%) obese subjects, 16 (33.3%) smokers, 11 (22.9%) subjects with hypertension, 12 (25%) subjects with dyslipidemia and 7 (14.6%) subjects with diabetes mellitus. In males of Group 3, the mean VFV/SFV was 0.93 0.28 and mean abdominal aortic calcium score
according to agatston scoring was 369 644.6 au. There were 50 (39.4%) obese subjects, 48 (37.8%) smokers, 33 (26%) subjects with hypertension, 36 (28.3%) subjects with dyslipidemia and 29 (22.8%) subjects with diabetes mellitus. In females of Group 3, it was determined that mean VFV/SFV was 1.1 0.87 and mean abdominal aortic calcium score according to agatston scoring was 356.2 363.1 au. There were 5 (27.8%) obese subjects, 3 (16.7%) smokers, 9 (50%) subjects with hypertension, no subject with dyslipidemia and 3 (16.7%) subjects with diabetes mellitus. Among all participants, SFV was 247.2 114.8 cm3, VFV was 160.5 62.1 cm3 and AaCs was 253.3 562.3 au in male subjects, whereas SFV was 355.8 139.7 cm3, VFV was 170.2 137.9 cm3 and AaCs was 188.7 422.5 au in female subjects. Whilst mean AaCs was statistically significantly higher in males versus females, mean SFV was statistically significantly higher in females versus males. You can see mean AaCS according to age in male patient in Figure 4(a) and in female patient in Figure 4(b). In the present study, the number of hypertensive patients was determined to be the highest in Group 3. The difference between the groups in terms of hypertension was statistically significant (p < 0.05) (p ¼ 0.006). Participants with dyslipidemia were more prevalent in Group 3. Statistically significant difference was determined between the groups in terms of dyslipidemia (p < 0.05) (p ¼ 0.04). Analysis concerning Type 2 diabetes mellitus revealed that number of type 2 diabetic patients was higher in Group 3 as compared to the other groups. The difference between the groups in terms of Type 2 diabetes was found to be statistically
Figure 4. (a) Mean AaCS according to age in male patients; (b) Mean AaCS according to age in female patients. AaCs: Abdominal Aortic Calcium Scoring; au: Agatston units.
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significant (p < 0.05) (p ¼ 0). The mean VFV was found low in the subjects with low mean AaCs (Group 1), whereas mean VFV was found high in the subjects with high mean AaCs (Group 3) and the difference was statistically significant (p < 0.01) (p ¼ 0). Data of the groups and results of statistics are demonstrated in Table 1.
Discussion Abdominal SFV and VFV were measured via MSCT and their relation with abdominal aortic calcium score, which is considered as atherosclerosis marker, was investigated in the subjects who participated in the present study. Statistically significant difference was determined between Group 3 and Group 2 (p < 0.05) (p ¼ 0.01) and between Group 3 and Group 1 (p < 0.01) (p ¼ 0.001) in terms of mean AaCs; whereas the difference between Group 2 and Group 1 was found to be statistically insignificant (p > 0.05) (p ¼ 0.69). It was found that the difference between the groups in terms of mean SFV was statistically significant, but relation with AaCs was statistically insignificant. Statistically significant difference was determined between Group 1 and Group 2 (p < 0.01) (p ¼ 0) and between Group 1 and Group 3 (p < 0.01) (p ¼ 0) in terms of mean VFV; whereas the difference between Group 2 and group 3 was found to be statistically insignificant (p > 0.05) (p ¼ 0.22). In the literature many studies exist regarding fat content. In these studies VFV and SFV was measured using CT. The comparison of visceral adipose tissue and subcutaneous adipose tissue has revealed that cardiometabolic risk factors have been found to be more associated with VFV.16–18 Rosenquist et al.19 investigated the interaction between cardiometabolic risks and visceral fat and subcutaneous fat tissue. According to the aforementioned study, they found that the increase in the VFV and SFV will intensify the cardiometabolic risks. Many studies found that increase in the amount of visceral adipose tissue is associated with dyslipidemia, type 2 diabetes, systemic inflammation and hypertension.20–25 Some studies focused on human adipose tissue vascularity and angiogenic properties.26,27 Several studies demonstrated inverse correlation between systemic insulin resistance indicators and average adipose tissue volume with the evaluation of fat biopsies.28,29 Recent studies regarding visceral and subcutaneous adipose tissue showed that BMI and morbid obesity decreased the angiogenic potential of adipose tissue.15–27 It is also stated in the literature that adipose tissue may increase cardiometabolic risks via inflammation and macrophage accumulation.31–32
Alexandersen et al.33 determined correlation between aortic calcified plaque measurements on lateral x-ray and truncal fat mass measured on x-ray absorptiometry in 168 male patients that had serious abdominal aortic calcified plaque.33 Whereas only serious abdominal aortic calcified plaque can be measured on x-ray, MSCT could have measured millimetric calcified plaques in the present study. The mean VFV was found low in the subjects with low mean AaCs (Group 1), whereas mean VFV was found high in the subjects with high mean AaCs (Group 3) and the difference was statistically significant (p < 0.01) (p ¼ 0). Anthropometric measurements may be unable to differentiate between VFV and SFV. Results of correlation between anthropometric measurements and subcutaneous and VFVs show difference in the studies carried out in different ethnic groups.34,35 No correlation was found between BMI and VFV in the South Asian populations.36 In the present study, no correlation was determined between BMI and VFV and between BMI and SFV. In the literature, there are different results concerning correlation between BMI and SFV and VFV. We believe that abdominal fat distribution should be measured by a direct and precise method such as MSCT and magnetic resonance imaging (MRI) for potential cardiometabolic results.
Conclusion Based on the results of present study, the first finding that would contribute to the literature is the notable increase observed in the risk of aortic atherosclerosis in Group 3. The second finding is the absence of significant correlation found between SFV and abdominal atherosclerosis. The last finding is statistically significant relation found between abdominal aortic atherosclerosis and abdominal VFV. We believe that determination of visceral and SFVs during routine abdominal MSCT scanning and informing the subjects in risky groups about cardiometabolic diseases would be beneficial.
Study limitations In the present study, the amounts of abdominal visceral fat tissue and subcutaneous fat tissue have been measured in a single section and as volume. Total amount of abdominal fat has not been studied in volumes. Furthermore, study participants were all from the same geographical region and were all Caucasians; thus, they do not represent other ethnic groups or different geographical regions. In some races such as Japanese Americans and Southeastern Asians, expected VFVs are higher as compared to BMIs.37 Therefore, larger epidemiological studies that would be performed
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in different geographical regions are needed to confirm the results of present study. Acknowledgments We thank Assoc. Prof. Ismail Keskin, PhD (Selc¸uk University, Zootechnics Division, Department of Biometry and Genetics, Konya, Turkey), for his contributions to the evaluation of results and statistical analysis.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Conflict of Interest None declared.
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