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DOI:10.2214/AJR.07.2366
AJR 2007; 189:1545-1553
© American Roentgen Ray Society

Review

Sonographic Assessment of Regional Adiposity

Ioannis S. Vlachos1, Achilleas Hatziioannou2, Apostolos Perelas1 and Despoina N. Perrea1

1 Department of Experimental Surgery and Surgical Research N. S. Christeas, Medical School of Athens, University of Athens, 15b Ag. Thoma str, 115 27, Goudi, Athens, Greece.
2 Department of Radiology, Areteion Hospital, Medical School of Athens, University of Athens, Athens, Greece.

Received April 3, 2007; accepted after revision June 24, 2007.

 
Cofunded by the European Social Fund and national resources (Operational Program for Educational and Vocational Training II—EPEAEK II, Project PYTHAGORAS II).

Address correspondence to D. N. Perrea (dperrea{at}med.uoa.gr).


Abstract
Top
 Abstract
Introduction
 Sonographic Indexes
 Comparisons of Indexes
 Conclusions
 References
 
OBJECTIVE. Various noninvasive imaging techniques, including CT, MRI, and sonography, have been used for accurate estimation of regional fat deposits. Among these techniques, sonography has attracted considerable attention because it combines safety, cost-effectiveness, and accuracy. The aim of this review is to present an overview of the studies in which sonographic techniques have been used to estimate visceral adiposity, the indexes derived, and the correlation between the indexes and metabolic and cardiovascular markers.

CONCLUSION. It is highly plausible that sonography will be used in clinical practice for the routine assessment of regional adiposity.

Keywords: abdominal wall fat index • adipose tissue • epicardial fat • intraabdominal thickness • mesenteric fat • obesity • preperitoneal fat


Introduction
Top
 Abstract
 Introduction
Sonographic Indexes
 Comparisons of Indexes
 Conclusions
 References
 
Obesity, defined by the World Health Organization as a body mass index (weight in kilograms divided by the square of height in meters) of 30 or greater, has emerged as a pandemic in the developed and developing parts of the world [1]. Obesity has been linked to diabetes mellitus, hypertension, stroke, hyperlipidemia, gallbladder disease, osteoarthritis, sleep apnea, and several types of cancer [2–5]. Moreover, obesity is causally related to cardiovascular disease (CVD) and is a major predictor of cardiovascular disorders [6, 7]. Although the detrimental health effects of obesity are well known, it also is becoming clear that regional fat distribution is a more important index of cardiovascular and metabolic deterioration than is total mass or volume of fat [8].

Regional adiposity can be assessed with anthropometric data and imaging techniques. The former include waist-to-hip ratio, waist circumference, and abdominal sagittal diameter. These measurements are easily obtained and cost-effective, do not involve ionizing radiation, and correlate with metabolic markers and imaging estimates [9]. For these reasons, the measurements have been widely accepted as indicators of intraabdominal fat deposition [10]. They are characterized, however, by low accuracy and reproducibility [10, 11]. Imaging techniques include CT, MRI, and sonography. CT is considered the reference standard for evaluation of adipose tissue [9]. However, it is relatively expensive and involves ionizing radiation. MRI does not involve ionizing radiation but is characterized by lower availability and high cost, and fat deposits tend to be overestimated [12, 13]. MRI and CT measurements are highly reproducible and allow assessment of fat deposit volumes with multislice approaches [9].

The use of sonography for the determination of fat distribution was introduced by Armellini et al. [14]. In a study with obese women, those investigators found a strong correlation between visceral fat thickness estimated with sonography and visceral adipose tissue area measured with CT. Further studies established the accuracy and repeatability of sonographic measurement of visceral thickness in various patient groups [15–17] and the correlation of sonographic measurements with CT- and MRI-based estimates [16, 17]. Sonographic measurements have been associated with metabolic values and central adiposity more strongly than have anthropometric data [16, 18–20].


Sonographic Indexes
Top
 Abstract
 Introduction
 Sonographic Indexes
Comparisons of Indexes
 Conclusions
 References
 
Since 1990, a number of indexes have been proposed to fully exploit the potential of sonography in the assessment of fat distribution. These indexes include intraabdominal fat thickness, maximum preperitoneal fat thickness, minimum subcutaneous fat thickness, epicardial fat thickness, and mesenteric fat thickness.

Intraabdominal Fat Thickness
The first sonographic index used for evaluation of visceral adiposity was intraabdominal or visceral fat thickness, defined as the distance between the anterior wall of the aorta and the posterior surface of the rectus abdominis muscle. Intraabdominal fat thickness is usually measured with a 3.5-MHz [21–23] or 3.75-MHz probe [24] 1–5 cm above the umbilicus at the xiphoumbilical line or midway between the xiphoid process and the umbilicus [25] (Figs. 1, 2, and 3). A number of researchers have used the distance between the spine and the rectus abdominis muscle [16, 22, 26] and the distance between the peritoneum and the lumbar spine [19]. All these measurements are highly reproducible with maximal reported intraobserver and interobserver variation coefficients of 6.5% [24] and 7% [16], respectively. Levels of intraabdominal fat thickness correlate with CT-based estimations of visceral fat [16–18, 21, 23, 24, 27–29] better than anthropometric measurements do [23], and the association is evident even in patients who have undergone gastric banding [18]. The value of the sonographic method was questioned only in a study of adolescents in the postpartum period [26]. Intraabdominal fat thickness correlates with subcutaneous fat estimates [24], and with the ratios of visceral to subcutaneous fat area and of visceral fat to muscle area. A cutoff value of 6.9 cm has been proposed [21] to discriminate between visceral and subcutaneous adiposity in women. This value had a sensitivity of 69.2% and specificity of 82.8% in making that determination.


Figure 1
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  		Fig. 1 —Drawing shows locations of maximum preperitoneal fat thickness, minimum subcutaneous fat thickness, abdominal wall fat index, and intraabdominal fat thickness measurements.

 

Figure 2
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  		Fig. 2 —Drawing shows anatomic landmarks for sonographic estimation of intraabdominal thickness.

 

Figure 3
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  		Fig. 3 —Sonogram corresponding to Figure 2 shows estimation of intraabdominal fat thickness in healthy middle-aged man.

 

As far as cardiovascular risk factors are concerned, intraabdominal fat thickness has been shown to correlate with total cholesterol and fasting glucose levels in men and women at high risk of CVD [19], apolipoprotein B and fasting insulin levels in obese women [27], and high-density lipoprotein (HDL) cholesterol and triglyceride (TG) levels in diabetic men and women and those at high risk of CVD [19, 27, 29]. Furthermore, intraabdominal fat thickness has been correlated with results of homeostatic model assessment for insulin resistance in diabetic patients and obese women [27, 29] and with plasma hemostatic factors in healthy men [23]. In diabetic patients, visceral fat thickness has been positively associated with the level of high-sensitivity C-reactive protein in both sexes and with carotid intimal–medial thickness (IMT) in men [29]. Visceral fat thickness also has been linked to ceruloplasmin level, a potent index of coronary artery disease [22].

In general, intraabdominal fat thickness is related to cardiovascular risk in specific subgroups of healthy volunteers and diabetic patients [19, 22, 23, 27, 29], although it is more sensitive than waist circumference and abdominal sagittal diameter in screening of men and women at high risk and of women at moderate risk [24]. In a multivariate analysis by Leite et al. [24], intraabdominal fat thickness was found the most significant marker of CVD in both sexes. Cutoff values of 7 and 9 cm successfully differentiated men at moderate and high risk, respectively, of CVD [24]. The corresponding values for women were 7 and 8 cm [24]. Intraabdominal fat thickness independent of age, sex, and body mass index has been found a significant predictor of the presence of metabolic syndrome (MS) [19]. Among diabetic patients, however, cutoff values of 47.6 mm for men and 35.5 mm for women had satisfactory sensitivity (71% and 69%, respectively) and specificity (74% and 78%, respectively) for the presence of MS [29].


Figure 4
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  		Fig. 4 —Drawing shows anatomic landmarks for sonographic estimation of maximum preperitoneal fat thickness and minimum subcutaneous fat thickness.

 


Figure 5
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  		Fig. 5A —Estimation of maximum preperitoneal fat thickness and minimum subcutaneous fat thickness. (Reprinted with permission from [36]) Sonogram shows thickened subcutaneous fat (S). P = preperitoneal fat.

 


Figure 6
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  		Fig. 5B —Estimation of maximum preperitoneal fat thickness and minimum subcutaneous fat thickness. (Reprinted with permission from [36]) Sonogram shows thickened preperitoneal fat (P). S = subcutaneous fat.

 
Abdominal Wall Fat Index
One of the most widely used sonographic indexes for estimation of regional adiposity is the abdominal wall fat index [20, 30–38]. For the assessment, subjects are placed in the supine position with shoulders, heels, and buttocks in contact with the examination bed. The thicknesses of subcutaneous and preperitoneal fat are measured by placement of a 7.5-MHz [29] or 3.75-MHz [36] probe perpendicular to the skin on the epigastrium. Longitudinal scans are obtained along the middle line (linea alba). The thickness of the subcutaneous fat is defined as the distance between the anterior surface of linea alba and the fat–skin barrier. The preperitoneal fat extends from the anterior surface of the liver (left lobe) to the posterior surface of linea alba. The minimum subcutaneous and maximum preperitoneal fat thicknesses are located immediately below the xiphoid process [36] (Figs. 1, 4, 5A, and 5B).

The abdominal wall fat index is the ratio of maximum preperitoneal to minimum subcutaneous fat thicknesses. It was proposed by Suzuki et al. [36] as the sonographic index exhibiting the strongest correlation with the CT-measured ratio of visceral to subcutaneous fat area. This index is characterized by excellent reproducibility and repeatability; in all studies the coefficient of variation has been reported to be less than 6% [20, 30, 36, 38].

On the basis of abdominal wall fat index measurements, obese persons can be further divided into those with prominent visceral (abdominal wall fat index > 1) or subcutaneous (abdominal wall fat index < 1) fat deposits. The former have been found to have elevated TG and total cholesterol levels and decreased flow-mediated vasodilatation, features indicative of elevated cardiovascular risk, despite a lower body mass index [30]. Among the components of the ratio, preperitoneal fat thickness is more frequently elevated in men and subcutaneous fat thickness in women [20, 29, 39]. Consequently, abdominal wall fat index tends to be higher in men [20, 29, 37, 39]. Abdominal wall fat index is correlated with carotid IMT in women [31] and is elevated in lean men [32] and in diabetic men and women [39]. Findings regarding the association between abdominal wall fat index and IMT in lean men, however, are controversial [32, 38]. These discrepancies can be attributed to differences in sample features, sample sizes, and study designs. Moreover, abdominal wall fat index is positively correlated with systolic blood pressure; diastolic blood pressure; TG, low-density lipoprotein (LDL) cholesterol, and total cholesterol levels; atherogenic index; and basal insulin levels in both sexes [31, 33, 36]. It is negatively correlated with HDL cholesterol level [36] and insulin sensitivity and leptin level in lean, obese, and hyperlipidemic men [20, 34–36]. In obese men, abdominal wall fat index has had an inverse correlation with flow-mediated increases in vessel diameter [30] and coronary flow velocity reserve [34]. It must be emphasized, however, that the foregoing associations have not been confirmed in certain patient groups. Abdominal wall fat index has not had a significant correlation with insulin sensitivity, HDL cholesterol level, carotid IMT, or even CT-obtained measurements of visceral fat in diabetic men or women [29].

Preperitoneal Fat Thickness
Although abdominal wall fat index is a well-established index among obese persons, its diagnostic value is limited among lean generally healthy persons and persons with diabetes [37–40]. In lean patients, the subcutaneous fat layer tends to be very thin, leading to abnormally high values of abdominal wall fat index and impairing its diagnostic accuracy [38]. In these cases, the total amount of visceral fat, represented by maximum preperitoneal fat, is better correlated with metabolic [37] and CVD risk factors [37, 38]. The index is elevated in patients with diabetes mellitus [39], and high levels of maximum preperitoneal fat have been associated with disease severity, increased CVD risk, and poor prognosis, as shown by the high prevalence of hypertension, microalbuminuria, retinopathy, and elevated levels of hemoglobin (A1c) [39]. A positive correlation exists between maximum preperitoneal fat thickness and urinary C-reactive protein or insulin level [39]. Preperitoneal fat thickness is also positively correlated with IMT [38], fasting insulin level [38], TG level [37, 38], CT-determined visceral fat area [36], coronary arterial stenosis score [37], fasting blood glucose level [37], and total and LDL cholesterol levels [37]. It is negatively correlated with HDL cholesterol level in lean men [37]. This index in lean women has limited value [37].

Subcutaneous Fat
In the limited number of studies in which it has been used, minimum subcutaneous fat thickness has been associated with LDL, HDL, and total cholesterol levels [37], although not as strongly as maximum preperitoneal fat thickness [37]. Minimum subcutaneous fat thickness also has been correlated with serum leptin level [39, 40].

Epicardial Adipose Tissue
Epicardial adipose tissue is a distinct type of visceral fat and shares its embryonic origin with intraabdominal fat [41]. Epicardial adipose tissue is directly attached to the heart, from which it is not separated by fascia, and has the same blood supply [42]. The secretory properties of epicardial adipose tissue are similar to, yet distinct from, those of visceral adipose tissue. In patients with CVD, epicardial adipose tissue expresses and secretes many inflammatory mediators, including interleukin 1ß, interleukin 6, monocyte chemoattractant protein 1, tumor necrosis factor {alpha}, and resistin [42–47], to a much greater extent than does subcutaneous fat. This disrupted adipokine release profile is believed to contribute to the pathogenesis of CVD and is accompanied by increased macrophage infiltration and thickening of the connective tissue septa [43, 44]. Epicardial fat deposits are more abundant on the free wall of the right ventricle and can be best measured there on long- and short-axis parasternal views [48] without being affected by hypertrophy of the right ventricle trabecula and moderator band.

In studies involving obese and nonobese men and women, Iacobellis et al. [48, 49] found that epicardial fat thickness ranged from 1.8 to 16.5 mm with an intraobserver variation coefficient of approximately 3% [49]. Sonographic measurements of epicardial adipose tissue correlated strongly with MRI estimates of epicardial and visceral fat deposits and with waist circumference, thigh circumference, and bioimpendance-determined body fat mass [48, 49]. The amount of epicardial adipose tissue was elevated in subjects of both sexes with visceral adiposity, even in the absence of MS [48, 49] and correlated with fasting insulin level, fasting glucose level, systolic and diastolic blood pressure, and LDL and HDL cholesterol and adiponectin levels [48]. Further studies involving obese persons confirmed the association between the amount of epicardial adipose tissue and parameters of MS. Epicardial fat thickness correlated with most insulin resistance and glucose intolerance indexes [50]. Chaowalit et al., however, found no association between epicardial fat thickness and coronary angiographic findings [51].

Mesenteric Fat Thickness
The most recently developed sonographic index for assessment of regional adiposity is mesenteric fat thickness. During a complete survey with emphasis on the paraumbilical area, the mesenteric leaves are recognized as elongated structures with highly reflecting peritoneal surfaces [52, 53] (Fig. 6). Sonography is the only imaging technique that depicts individual mesenteric leaves. Maximal thickness is estimated, and the mean of the three thickest leaves is calculated [54]. The measurements are characterized by high intraoperator and interoperator reliability [54].


Figure 7
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  		Fig. 6 —Mesenteric leaves. Sonogram shows maximum mesenteric thickness (+... +) measured with calipers. Arrows indicate mesenteries. (Reprinted with permission from [53])

 
Mesenteric fat thickness is greater in men [54, 55] and is an independent predictor of sonographically determined preperitoneal and subcutaneous fat thicknesses [55] as well as of the presence of MS [55]. In community studies, the association between the amount of mesenteric adipose tissue and total cholesterol, LDL cholesterol, TG, fasting glucose, and hemoglobin A(1c) levels and systolic blood pressure in men [54] and TG and hemoglobin A(1c) levels in women [54] was higher than that between these metabolic parameters and maximum preperitoneal fat thickness, maximum subcutaneous fat thickness, total amount of abdominal or visceral fat estimated with MRI, body mass index, waist circumference, or waist-to-hip ratio [54]. After multiple regression analysis, mesenteric fat thickness was chosen as the major explanatory variable for increased TG, total cholesterol, LDL cholesterol, and hemoglobin A(1c) levels in men and increased TG level in women [54]. The odds ratio for MS increased by a factor of 1.35 for each 1-mm increase of mesenteric fat thickness [55].

Mesenteric fat thickness correlated with IMT in lean subjects [53], whereas persons with more than 10 mm of mesenteric adipose tissue had higher values of IMT [55]. In a multivariate analysis [55], mesenteric adipose tissue thickness was an independent determiner of all the components of MS after adjustment for the homeostatic model assessment for insulin resistance, preperitoneal and subcutaneous fat thicknesses, sex, and age. Moreover, a cutoff value of 10 mm had a sensitivity of 70% and a specificity of 75% in differentiating patients with and those without MS. The strong correlations observed between amount of mesenteric fat and metabolic or cardiovascular parameters can be attributed to the unique capability of sonography in direct assessment of portal fat, which is considered particularly atherogenic [54].

Preperitoneal Circumference
Preperitoneal circumference is a recently proposed index [56]. For this estimate, the patient is placed in a supine position, and a 7.5-MHz linear probe perpendicular to the skin is used for a longitudinal scan at the midpoint between the umbilicus and the xiphoid process on the linea alba. Subcutaneous fat thickness spans from the outer edge of linea alba to the inner edge of the skin. The preperitoneal circumference is calculated as the difference between waist circumference and the product of 2{pi} and subcutaneous thickness. It has been found to be correlated with all the components of MS (blood pressure, waist circumference, and fasting blood glucose, TG, and HDL levels) and with insulin resistance in healthy middle-aged volunteers [56].

Other Indexes
Certain other indexes have been used by researchers for sonographic estimation of regional adiposity. These indexes include the distance between the internal surface of the abdominal muscle and the splenic vein [57] and the thickness of the fat layer of the posterior right renal wall [57]. For acquisition of either index, patients are placed in a supine position, and at the end of a normal exhalation, the values are measured with a 3.5-MHz probe perpendicular on the skin. The distance between the abdominal muscle and the vein is scanned transversely in the midline. If the vein cannot be visualized clearly, it can still be detected with color Doppler flow imaging. Both indexes have been found to correlate with visceral fat volume [57].


Comparisons of Indexes
Top
 Abstract
 Introduction
 Sonographic Indexes
 Comparisons of Indexes
Conclusions
 References
 
Evaluation of the adiposity indexes is hindered by a lack of large comparison studies. However, remarks can be made on each index.

Intraabdominal Fat Thickness
Intraabdominal fat thickness seems to be the most reliable index. Although intraabdominal fat thickness is not as strongly associated with insulin sensitivity and cardiovascular risk factors as are epicardial adipose tissue and mesenteric fat thickness, its value and reproducibility have been repeatedly confirmed in a large number of studies by different research groups examining diverse populations and patient groups (Tables 1, 2, 3, 4).


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  		TABLE 1: Correlation Between Adiposity Indexes and Homeostatic Model Assessment for Insulin Resistance

 

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  		TABLE 2: Correlation Between Adiposity Indexes and High- and Low-Density Lipoprotein Cholesterol Levels

 

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  		TABLE 3: Correlation Between Adiposity Indexes and Carotid Intimal-Medial Thickness

 

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  		TABLE 4: Correlation Between Adiposity Indexes and Analogous CT and MRI Indexes

 

Abdominal Wall Fat Index
The abdominal wall fat index is the only index that is a direct assessment of fat distribution. This index, however, is based on measurement of maximum preperitoneal fat thickness, a fat deposit that is not considered visceral fat tissue, hindering its use and diagnostic value. The abdominal wall fat index has been used extensively and it has had significant correlation with CT estimates (Table 4). Associations between abdominal wall fat index and metabolic values (Table 1) and cardiovascular risk factors (Tables 2 and 3) have not been confirmed in all patient populations. Data indicate that the utility can be maximized if the abdominal wall fat index is measured in specific groups, such as obese patients and those with hyperlipidemia.

Preperitoneal Fat
Preperitoneal fat extrudes to the systemic blood circulation rather than the portal vein and is not considered a type of visceral fat. Measurement of preperitoneal fat thickness, however, seems a good alternative to calculation of abdominal wall fat index in lean persons, in whom higher values of abdominal wall fat index do not necessarily correspond to elevated cardiovascular risk. The relatively smaller values of the denominator (minimum subcutaneous fat) result in abnormally higher values of the ratio. Because assessment of maximum preperitoneal fat thickness is essential for estimation of abdominal wall fat index, it is possible that combined evaluation may result in a higher diagnostic value, but this hypothesis has not been confirmed.

Mesenteric Fat Thickness
From a pathophysiologic point of view, mesenteric fat thickness is a notably promising index. Mesenteric fat extrudes to the portal vein, enabling its secretory products (e.g., adipokines and free fatty acids) to directly affect liver function, blood lipid levels, and insulin resistance. Mesenteric fat thickness has had the strongest correlations with insulin sensitivity (Table 1) and carotid IMT (Table 3) and has had significant correlations with blood lipid measurements (Table 2). Despite these encouraging data and the strong pathophysiologic background, the use of mesenteric fat thickness has been examined in only a small number of studies. Further research is needed to establish the diagnostic value of the mesenteric fat index.

Epicardial Adipose Tissue
Epicardial fat is directly attached to the heart, and this proximity potentiates the effects of epicardial adipose tissue–derived agents on coronary vasculature and myocardial cells. The amount of epicardial adipose tissue has had the strongest associations with HDL and LDL cholesterol levels (Table 2) and impressive correlations with MRI measurements (Table 4). Moreover, the most important advantages of measuring epicardial adipose tissue are the considerably straightforward measurement technique and cost-effectiveness. A cardiologist using a standard transducer can estimate the amount of epicardial adipose tissue during a routine sonographic examination. As in the case of mesenteric fat thickness, the most important disadvantage of this index is the small number of studies in which it has been examined.


Conclusions
Top
 Abstract
 Introduction
 Sonographic Indexes
 Comparisons of Indexes
 Conclusions
References
 
Sonographic assessment is a good alternative to both sophisticated imaging techniques and collection of anthropometric data. Sonography is noninvasive, painless, safe, accurate, reproducible, and cost-effective, and it does not expose patients to ionizing radiation. Sonographic assessment can be performed on children and pregnant women and can be used in extensive screening studies. Sonographic results correlate strongly with those of much more expensive imaging techniques, and the use of specialized indexes contributes to direct assessment of cardiovascular and metabolic risk. Selection of the proper cutoff values for patients in different groups has led to promising results regarding the noninvasive diagnosis of MS and evaluation of cardiovascular risk status.

Despite the advantages, use of sonography for assessment of body composition is accompanied by important disadvantages. The accuracy is low among postpartum adolescents, patients with ascites, and patients who have undergone operations on the epigastric region. Sonography entails use of equipment and is significantly more expensive than simple assessment of anthropometric features. Although the value of sonography has been shown in most studies, sporadic reports question the strong association between sonographic findings and those of standard techniques [26] and clinical outcome [51]. There is also an evident need for objective and accurate indexes that can be applied to special patient groups. Furthermore, adequate examiner training is demanded as a precondition for reliable and reproducible measurements. Once these issues are resolved, it is highly plausible that sonography will be used in clinical practice for the routine assessment of regional adiposity.


Acknowledgments
 
We thank Th. Xanthos for expert advice and useful comments and A. Bampali for assistance.


References
Top
 Abstract
 Introduction
 Sonographic Indexes
 Comparisons of Indexes
 Conclusions
 References
 

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