Obesity is an abnormal or excessive fat accumulation

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1 /STRU^NI RAD UDK 617.5: DOI: /ACI D Ultrasonographic evaluation of visceral and subcutaneous abdominal fat tissue before and after bariatric surgery... Djuri}-Stefanovi} A. 1,3, Vasin D. 1, Jovanovi} S. 1, Lazi} Lj. 1, Kova~ J. 1,3, Popovi} I. 1, Bajec Dj. 2,3, [aranovi} Dj. 1,3 1 Unit of Digestive Radiology (First Surgical Clinic), Center of Radiology and MR, Clinical Center of Serbia 2 Clinic of Digestive Surgery (First Surgical Clinic), Clinical Center of Serbia 3 Faculty of Medicine, University of Belgrade Visceral fat is considered a key factor in the development of metabolic syndrome and other pathological conditions and diseases associated with obesity. Therefore, analysis of the dynamics of reducing the amount of abdominal visceral fat is important for evaluating the therapeutic effects of different modalities of obesity treatment, including bariatric surgery. In 53 obese patients visceral and subcutaneous abdominal adipose tissue was measured by ultrasonography (US) before and after bariatric surgery, in the period of 1, 3, 6 months. At the same time, standard anthropometric parameters were assessed: body mass (m), BMI, waist circumference (WC), and hip circumference (HC). Five diameters of the visceral abdominal fat (VAF) were measured: IAFT (Intraabdominal Fat Thickness), LV (Lienal Vein), VF (Visceral Fat), MES sum (Mesenterial leafs) and Max PFT (Maximal Preperitoneal Fat Thickness), and three diameters of the subcutaneous abdominal adipose tissue (SCAF): Min SFT (Minimal Subcutaneous Fat), and MaxSFTa and MaxSFTb (Maximal Subcutaneous Fat Thickness a and b). Statistically significant decrease in all anthropometric parameters, except HC was registered 1, 3 and 6 months after the surgery. We registered the decline of almost all US diameters of abdominal adipose tissue in the follow-up period, but statistically significant decrease were found only in the diameters of visceral adipose tissue: IAFT after 1 and 3 months (p=0.031 and p=0.027); VF after 1 month (p=0.031), LV after 6 months (p=0.011), and MESsum after 3 and 6 months (p=0.001 and p=0.028), as well as MaxSFTb, at 1 month follow-up (p=0.015). In the short-term follow-up period after the bariatric surgery, there was a significant decrease in body mass, BMI and WC, and ultrasonography revealed a significant reduction in the diameters of the visceral abdominal fat. Key words: obesity, ultrasonography, fat tissue, bariatric surgery. rezime INTRODUCTION Obesity is an abnormal or excessive fat accumulation in the body, which threatens the health and is, as recent studies show, irreversible condition, without medical treatment. 1 The most commonly used parameter for quantifying obesity is the body-mass index (BMI). People whose BMI is 30 kg/m 2 or more, qualify as obese. BMI over 40 kg/m 2 indicates severe or morbid obesity. 1 Obesity is considered a predisposition to the development of many cardiovascular and cerebrovascular risk factors diseases such as hypertension, dyslipidemia, diabetes, metabolic syndrome, as wll as the development of musculoskeletal di-sorders or some types of cancer. 2 One of the available me-thods for the quantification of obesity is to assess the amount of abdominal fat, which could be done in two ba-sic ways: anthropometric measurements (mass, BMI, wa-ist circumference, hip circumference and the ratio of these two values, the upper arm circumference), and radiological imaging methods (computed tomography, ultrasonography, magnetic resonance imaging). 3-9 Abdominal adipose tissue is divided into two compartments: subcutaneous and visceral. 3-5 Visceral adipose tissue is located inside the abdominal cavity. It surrounds organs of the abdominal cavity, and the smaller part is located in the visceral abdominal organs. Extensive Framingham s study of cardiovascular risk factors showed that increased accumulation of the visceral fat in the abdomen is related to complications of obesity such as type 2 diabetes and coronary artery disease. 2 It was also shown that the correlation between the quantity of visceral fat and atherosclerosis is not dependent on age, overall obesity or subcutaneous adipose tissue volumes. 2 Recent studies suggest different physiological behavior of visceral and subcutaneous adipose tissue. 3 The amount and ratio of two compartments differ depending on gender and ethnicity. 6 It has been reported that there is bigger amount of visceral fat in males, African-American women, Japanese and Indians. 6

2 26 A. Djuric-Stefanovic et al. ACI Vol. LX There are two therapeutic approaches in the treatment of obesity: conservative and surgical. Conservative treatment includes the use of low-calorie diet and drugs. Surgical treatment is indicated if the BMI is higher than 40 kg/m 2, or if the BMI is higher than 35 kg/m 2, with associated diseases (diabetes, hypertension, hyperli-pidemia, etc.). 7 There are few techniques of bariatric surgery, but mostly used are: laparoscopic Roux-and-Y gastric bypass gastroplasty, vertical " band " gastroplasty, laparoscopic "banding" and stomach "sleeve" gastrectomy. 7 It is expected that the body weight decrease after the bariatric surgery, which correlates with a decrease of the total body fat amount. Ultrasonography is an effective method of quantification of subcutaneous and visceral fat, even when compared with the methods of the "gold standard" in this type of radiological diagnosis: computed tomography and magnetic resonance imaging. 7 The purpose of this study was to monitor the dynamics of the decrease of amount of abdominal fat in obese patients after the bariatric surgery by measuring certain diameters with ultrasonography, which could indicate the quantity and distribution of two different compartments of abdominal fat : subcutaneous and visceral. PATIENTS AND METHODS Between June and Februar 2012., ultrasonographic measurements were performed in 53 obese patients (41 women and 12 men, mean age 40 (+11) years, years), who were operated within the next 1-3 days. All ultrasound examinations were performed at the Center of Digestive Radiology and MRI, Clinical Center of Serbia (First Sur-gical Clinic), with convex US probe, frequency of 3-5 MHz and linear ultrasound probe, frequency of 5-10 MHz, after adequate preparation of the patient (8 hours without a meal). At the same time, basic anthropometric parameters were measured: body mass (m), height (h), body mass index (BMI), waist circumference (WC) and hip circumference (HC) (Table 1). We measured five diameters of abdominal visceral fat (VAF ) : 1. IAFT (Intraabdominal Fat Thickness) - distance from the posterior surface of the rectus abdominis muscle to the anterior wall of the aorta, measured 2 cm above the umbilicus ( Figure 1A ) 2 LV (Lienal Vein) - distance from the posterior surface of the rectus abdominis muscle to the anterior wall of the lienal vein (Figure 1B) 3 VF (Visceral Fat) - distance from the back surface of the posterior surface of the rectus abdominis muscle to the paravertebral muscles, measured at the level of the umbilicus (Figure 2) 4 MES (Mesenterial leafs) - thickness of the three mesenterial leafs (superficial, middle, deep and sum), measured besides the umbilicus (MES 1, 2 and 3 and sum) (Figure 3 ) 5 MaxPFT (Maximal Preperitoneal Fat Thickness) - distance from the white line (linea alba) to the left lobe of the liver, as measured below the xyphoid processus (Figure 4). We also measured three diameters of the subcutaneous abdominal fat (SCAF) : 1. MinSFT (Minimal Subculaneous Fat) - the distance from the surface of the skin to the linea alba, measured below the xyphoid processus (Figure 4) TABLE 1 ANTHROPOMETRIC PARAMETERS (n=53), MEASURED BEFORE SURGERY Anthropometric parameters X+SD Min Max m (kg) h (m) BMI(kg/m 2 ) WC (cm) HC (cm) TABLE 2 ULTRASONOGRAPHIC DIAMETERS OF THE VAF AND SCAF BEFORE SURGERY (n=53) US diameters X+SD Min Max IAFT (mm) LV (mm) VF (mm) MES sum (mm) MaxPFT (mm) MinSFT (mm) MaxSFTa(mm) MaxSFTb(mm) MaxSFTa (Maximal Subculaneous Fat Thickness a) - the distance from the surface of the skin to the linea alba, measured 2 cm above the umbilicus 3 MaxSFTb (Maximal Subculaneous Fat Thickness b) - the distance from the surface of the skin to the linea alba, measured 2 cm below the umbilicus. All patients were operated at the Clinic of Digestive Surgery (First Surgical Clinic), Clinical Center of Serbia. Laparoscopic Roux - and- Y gastric bypass gastroplasty was performed. Control ultrasonographic examinations were performed following the same protocol as the initial, 1, 3 and 6 months after the surgery in patients who came to the scheduled check-ups. Statistical analysis was performed using the statistical package SPSS for Windows Data obtained by ultrasound measurements are presented in mean and standard deviation, and maximum and minimum value (mean+/- SD, Max, Min), after testing the normality of distribution using the Shapiro-Wilk test. To compare values of the corresponding diameters of visceral and subcutaneous abdominal adipose tissue from the same patient, at the initial and control examination, the paired samples t- test was used (t). Values of p <0.05 were considered statistically significant..

3 Br. 3 US evaluation of visceral and subcutaneous abdominal fat 27 tissue before and after bariatric surgery TABLE 3 CHANGE OF THE ANTHROPOMETRIC PARAMETERS DURING THE POSTOPERATIVE FOLLOW-UP Anthropometric X+SD initially vs. X+SD1/3/6 months parameters 1 month (n=12) 3 months (n=6) 6 months (n=4) m (kg) vs ** p< vs ** p< vs 99+16* p=0.013 BMI (kg/m 2 ) vs ** p< vs ** p< vs ** p=0.009 OS (cm) vs 117+7** p< vs * p< vs 110+7* p=0.017 OK (cm) vs p= vs 133+9* p= vs * p=0.062 **:p<0.01; *:p<0.05 TABLE 4 CHANGE OF THE US DIAMETERS DURING THE POSTOPERATIVE FOLLOW-UP X+SD initially vs. X+SD1/3/6 months US diameters 1 month (n=16) 3 months (n=8) 6 months (n=4) IAFT (mm) vz 61+22* p= vs 43+16* p= vs p=0.240 LV (mm) vs p< vs p= vs 48+14* p=0.031 VF (mm) vs * p= vs p=0.510 MEZ sum (mm) vs p= vs 31+8** p= vs30+8* p=0.028 MacPFT(mm) 22+6 vs 22+7 p= vs 19+8 p= vs14+5 p=0.468 MinSFT(mm) 29+8 vs 29+9 p= vs24+5 p= vs23+5 p=0.058 MaxSFTa(mm) vs p= vs49+12 p= vs41+8 p=0.307 MacSFTb(mm) vs 56+15* p= vs58+21 p= vs49+8 p=0.807 **:p<0.01; *p<0.05 RESULTS Diameters of the VAF and SCAF those were measured by ultrasonography before the surgery in the whole group of patients (n=53), are summarized in Table 2. Of the total number of initially examined and operated patients, 28 patients arrived to the control US examination (1, 3, or 6 months after surgery). Statistically significant decrease in the majority of the anthropometric parameters was registered in the followup period of 1, 3 and 6 months after surgery (Table 3, Figure 5, and Figure 6). Control ultrasound revealed decrease of almost all diameters of the abdominal adipose tissue, which were measured, but statistically significant decrease was found only in some of the diameters of the visceral adipose tissue (Table 4). DISCUSSION Diagnostic follow-up of morbidly obese patients before and after bariatric surgery includes monitoring of anthropometric parameters: body weight, BMI, waist, hips, upper arm circumferences, and fat distribution. Computed tomography (CT) is considered the reference method for the accurate quantification of visceral and subcutaneous adipose tissue. 5 However, its use in extremely obese patients is limited. Since most of these patients are young, exposure to the ionizing radiation during the CT scanning is not negligible. It has been reported that CT and US corellate well in measuring the diameters of the abdominal sucutaneous and visceral fat. 5 It was also shown that values of some anthropometric parameters are not reliable indicators for the amount of the visceral fat. 6,7 In our series, there was significant decrease in the ultrasonographically measured diameters of visceral abdominal fat, compared to the diameters of the subcutaneous abdominal adipose tissue, in the short follow-up period (1-6 months after the surgery) (Table 4). Weiss et al found in their study, which included 27 patients who were examined by CT six months after bariatric surgery, that the decrease in the abdominal visceral fat was proportional to the decrease in the subcutaneos fat, which mean that the VAF/ SCAF index remained approximately unchanged 6 months after the surgery, although the decrease of both the VAF and the SCAF area was prouved. 10 We assume that the reason for (statistically) significant decrease of diameters of the visceral abdominal fat, but not of diameters of the subcutaneous fat, which we evaluated in our study, is in fact that the average lengths of the VFA diameters were greater the SCAF diameters (Table 2). Therefore, the differences in lengths of thevaf diameters could easier reach the statistical significance, compared with the SCAF diameters. In support of this hypothesis is the fact that, of all diameters of the subcutaneous fat, only statistically significant reduction of the MaxSCFb was revealed in the follow-up period, probably because the MaxSCFb represents the longest diameter of the subcutaneous abdominal adipose tissue (Tables 2 and 4). It could be

4 28 A. Djuric-Stefanovic et al. ACI Vol. LX marked that the shortest diameters, which were measured Max PFT and Min SFT, almost did not change at onemonth follow-up (Tables 2 and 4). In the study of Sabir et al, authors reported that the highest maximum diameter of the peritoneal adipose tissue was significantly decreased in obese women during a hypocaloric diet regime, which corresponds with MESsum diameter in our study. 11 Therefore, our results are in agreement with the results of the study of Sabir et al, because we have found a statistically significant difference in MESsum after three and six months, compared to the initial values (Table 4). In the study by Wirth et al, the authors found that visceral abdominal fat decreased significantly in men, while in women the amount of subcutaneous fat mostly decreased during the hypocaloric dietary regime. 12 It was not possible for us to do valid comparison of the dynamics of change in diameters of two abdominal fat compartments in relation to the sex in our study, because the patient population was too small. One drawback of this study was a relatively small number of patients who were followed-up. Second, the US examination were performed by three physicians, which could lead to a certain imprecision in the measurements, especially when using a linear ultrasound probe, because small differences in the degree of compression of linear ultrasound probe result in the difference in the measured diameter of up to several millimeters. Follow-up period was relatively short, so we believe that it would be useful to repeat the US evaluation of parameters of the abdominal fat in all operated patients at least one year after the operation, in order to evaluate the medium-term effects of the bariatric surgery. FIGURE 1A-B. US PRESENTATION OF THE PARAMETERS OF THE VISCERAL ABDOMINAL FAT: IAFT AND LV CONCLUSION Based on the initial results that we presented, we can conclude that ultrasound is a useful imaging method in monitoring of obese patients after bariatric surgery in order to exactly quantify the amount and proportion of two diff-erent compartments of the abdominal fat: visceral and subcutaneous. We believe that statistically significant decline of some of the US diameters of the visceral abdominal fat in patients who were undergoing bariatric surgery, during the short-term follow-up of 6 months, indicatied the therapeutic validity of bariatric surgery in morbidly obese and over-weight patients with associated obesityrelated diseases. SUMMARY ULTRASONOGRAFSKA EVALUACIJA VISCERALNOG I SUBKUTANOG ABDOMINALNOG MASNOG TKIVA PRE I POSLE BARIJATRIJSKE HIRURGIJE Visceralno masno tkivo se smatra klju~nim faktorom u razvoju metaboli~kog sindroma i drugih patoloških stanja i oboljenja koja su udru ena sa gojaznoš}u. Zbog toga je pra}enje dinamike smanjivanja koli~ine abdominalnog visceralnog masnog tkiva zna~ajno u proceni terapijskog efekta razli~itih modaliteta le~enja gojaznosti, u koje spada i barijatrijska hirurgija. U 53 gojazna pacijenta ultrasonografski je mereno subkutano i visceralno abdominalno masno tkivo pre i posle barijatrijske operacije, u vremenskom periodu od 1, 3 i 6 meseci. Istovremeno su kod istih pacijenata utvrdjivani i standardni antropometrijski parametri: telesna masa, BMI, obim struka (OS) i obim kuk- FIGURE 2. US PRESENTATION OF THE PARAMETERS OF THE VISCERAL ABDOMINAL FAT: VF ova (OK). Ultrazvu~no je mereno pet parametara koli~ine visceralnog abdominalnog masnog tkiva (VAF): IAFT (IntraAbdominal Fat Thickness), LV (Lienal Vein), VF (Visceral Fat), MEZsum (Mesenterial leafs) i MaxPFT (Maximal Preperitoneal Fat Thickness) i tri parametra koli~ine subkutanog abdominalnog masnog tkiva (SCAF): MinSFT (Minimal Subculaneous Fat), MaxSFTa i

5 Br. 3 US evaluation of visceral and subcutaneous abdominal fat 29 tissue before and after bariatric surgery FIGURE 3. THICKNESS OF THREE MESENTERIAL LEAFS (MES1, MES2, MES3). FIGURE 5. THE AVERAGE DECREASE IN BODY MASS (M) AF- TER THE BARIATRIC SURGERY. FIGURE 4. US PRESENTATION OF THE PARAMETERS OF THE VISCERAL AND SUBCUTANEOUS ABDOMINAL FAT, MEASURED BY LINEAR US PROBE: MINSFT AND MAXPFT MaxSFTb (Maximal Subculaneous Fat Thickness a and b). Statisti~ki zna~ajan pad svih antropometrijskih parametara, osim obima kukova, registrovan je 1, 3 i 6 meseci posle operacije. Kontrolnim ultrazvu~nim pregledima registrovano je smanjenje skoro svih dijametara abdominalnog masnog tkiva koji su mereni, ali je statisti~ki zna~ajan pad utvrdjen samo za neke od dijametara visceralnog masnog tkiva: IAFT posle 1 i 3 meseca (p=0,031 i p= 0,027); VF posle 1 meseca (p=0,031); LV posle 6 meseci (p=0,011); i MEZsum posle 3 i 6 meseci (p=0,001 i p= 0,028), kao i za MaxSFTb, posle 1 meseca (p=0,015). FIGURE 6. THE AVERAGE DECLINE IN BMI AFTER THE BARIA- TRIC SURGERY. U kratkoro~nom periodu pra}enja u trajanju od 6 meseci posle barijatrijske operacije, došlo je do zna~ajnog smanjenja telesne mase, BMI i obima struka, a ultrazvu~nim merenjem je detektovano zna~ajno smanjenje dijametara visceralnog abdominalnog masnog tkiva. Klju~ne re~i: gojaznost, ultrasonografija, masno tkivo, barijatrijska hirurgija. REFERENCES 1. Obesity: preventing and managing the global epidemic: report of a WHO consultation. World Health Organ Tech Rep Ser 2000; 894: Fox CS, Massaro JM, Hoffman U, Pok H, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham heart study. Circulation 2007; 116: Kobayashi J, Takeyoshi S, Watanabe M. The relationship of abdominal fat mass assessed by helical or conventional computed tomography to serum leptin concentration. Journal of atherosclerosis et thrombosis 2004; 11:

6 30 A. Djuric-Stefanovic et al. ACI Vol. LX 4. Vlachos IS, Hatzioannou A, Perelas A, Perrea D. Sonographic assessment of regional adiposity. Am J Roendgenol 2007; 189: Hirooka M, Kumagi T, Kurose K, et al. A technique for the measurement of visceral fat by ultrasonography: comparison of measurement by ultrasonography and computed tomography. Internal Medicine 2005; 44: Camhi SM, Brav GA, Bouchard C, et al. The Relationship of waist circumference and BMI to visceral, subcutaneous, and total body fat: sex and race differences. Obesity 2011; 19: Stolk RP, Meijer R, Mali WP, Grobbee DE, Graaf Y. Ultrasound measurement of intraabdominal fat estimate the metabolic syndrome better than do measurements of waist circumference. Am J Clin Nutr 2003; 77: Shuster A, Patlas M, Pinthus JH, Mourtzakis M. The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis. Br J Radiol 2012; 85: Pontiroli AE, Pizzocri P, Giacomelli M, et al. Ultrasound measurement of visceral and subcutaneous fat in morbidly obese patients before and after laparoscopic adjustable gastric banding: comparison with computerized tomography and with anthropometric measurements. Obesity Surgery 2002; 12: Weiss R, Appelabum L, Schweiger C, et al. Shortterm dynamics and metabolic impact of abdominal fat depots after bariatric surgery. Diabetes Care 2009; 32: Sabir N, Pakdemirli E, Sermez Y, et al. Sonographic assessment of changes in thickness of different abdominal fat layers in response to diet in obese women. Journal of Clinical Ultrasound 2003; 31: Wirth A; Steinmetz B. Gender differences in changes in subcutaneous and intra-abdominal fat during weight reduction: an ultrasound study. Obes Res 1998; 6:

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