Intra-abdominal fat. Part II: Non-cancerous lesions of the adipose tissue localized beyond organs

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VOLUME 16 , ISSUE 64 (March 2016) > List of articles

Intra-abdominal fat. Part II: Non-cancerous lesions of the adipose tissue localized beyond organs

Andrzej Smereczyński * / Katarzyna Kołaczyk / Elżbieta Bernatowicz

Keywords : intra-abdominal fat, non-cancerous lesions, fat necrosis, ultrasound imaging, differential diagnosis

Citation Information : Journal of Ultrasonography. Volume 16, Issue 64, Pages 32-43, DOI: https://doi.org/10.15557/JoU.2016.0004

License : (CC BY-NC-ND 3.0)

Received Date : 01-September-2015 / Accepted: 14-November-2015 / Published Online: 29-March-2016

ARTICLE

ABSTRACT

Adipose tissue does not belong to the most favorite structures to be visualized by ultrasound. It is not, however, free from various pathologies. The aim of this paper is to make abdominal cavity examiners more familiar with non-cancerous lesions found in intra-abdominal fat. The main focus is lesions that are rarely discussed in the literature. Visceral adiposity is one of important pathogenetic factors contributing to cardiovascular events, metabolic syndrome and even certain neoplasms. That is why this article exposes sonographic features that are the most characteristic of these lesions. The value of ultrasonography in the diagnosis of this pathology is underestimated, and a number of US scan reports do not reflect its presence in any way. Moreover, the article discusses more and more common mesenteritis, the lack of knowledge of which could pose difficulties in explaining the nature of symptoms reported by patients. Furthermore, this review presents lesions referred to in the literature as focal infarction of intra-abdominal fat. This section focuses on infarction of the greater and lesser omentum, epiploic appendagitis, mesenteric volvulus and focal fat necrosis resulting from pancreatitis. These lesions should be assessed with respect to the clinical context, and appropriate techniques of ultrasonography should be employed to allow careful determination of the size, shape, acoustic nature and location of lesions in relation to the integuments and large bowel, as well as their reaction to compression with an ultrasound transducer and behavior during deep inspiration. Moreover, each lesion must be obligatorily assessed in terms of blood flow. Doppler evaluation enables the differentiation between primary and secondary inflammation of intra-abdominal fat. The paper also draws attention to a frequent indirect sign of a pathological process, i.e. thickening and hyperechogenicity of fat, which sometimes indicates an ongoing pathology at a deeper site. This structure may completely conceal the primary lesion rendering it inaccessible for ultrasound. In such cases and in the event of other doubts, computed tomography should be the next diagnostic step.

Tkanka tłuszczowa nie należy do ulubionych struktur obrazowanych ultrasonograficznie, ale niestety nie jest wolna od różnorodnych patologii. Praca ma przybliżyć lekarzom badającym ultrasonograficznie jamę brzuszną zmiany nienowotworowe, które spotykane są w tłuszczu wewnątrzbrzusznym. Skupiono się głównie na zmianach rzadko omawianych w piśmiennictwie. Otłuszczenie trzewne to jeden z ważnych czynników patogenetycznych incydentów sercowo-naczyniowych, zespołu metabolicznego, a nawet niektórych nowotworów, dlatego w artykule wyeksponowano cechy sonograficzne najbardziej charakterystyczne dla symptomatologii tych zmian. Wartość ultrasonografii w rozpoznawaniu tej patologii jest niedoceniana i przez to w wielu wynikach USG nie znajduje żadnego odzwierciedlenia. Ponadto opisano coraz częściej spotykane zapalenia krezki, których nieznajomość będzie sprawiać kłopoty przy wyjaśnieniu natury dolegliwości odczuwanych przez chorych. Kolejnymi tematami tego opracowania są zmiany określane w piśmiennictwie jako ogniskowy zawał tłuszczu wewnątrzbrzusznego. W tej grupie patologii skupiono się na zawale sieci większej i sieci mniejszej, przyczepków sieciowych, skrętu krezki i ognisk martwicy tkanki tłuszczowej w następstwie zapalenia trzustki. W ocenie tych zmian należy brać pod uwagę kontekst kliniczny oraz odpowiednią metodykę badania USG polegającą na dokładnym określeniu wielkości, kształtu, charakteru akustycznego i lokalizacji zmian względem powłok oraz jelita grubego, a także ich podatności na ucisk głowicą oraz zachowania się w czasie głębokich oddechów. Ponadto każdą zmianę koniecznie należy ocenić pod względem unaczynienia. Na podstawie badania dopplerowskiego będzie można odróżnić od siebie pierwotne zapalenie tłuszczu wewnątrzbrzusznego od zapalenia wtórnego. W pracy zwrócono też uwagę na często spotykany pośredni objaw procesu chorobowego, którego przejawem jest pogrubiała i hiperechogeniczna tkanka tłuszczowa, niekiedy będąca wybijającym się objawem toczącej się głębiej patologii. Taka struktura może całkowicie kryć zmianę pierwotną, która przez to może być niedostępna badaniu USG. W tych przypadkach i przy innych wątpliwościach kolejnym krokiem diagnostycznym powinna być tomografia komputerowa.

Graphical ABSTRACT

As any other tissue in the human body, intra-abdominal fat is subject to various pathological processes which can be neglected because of the lack of appropriate knowledge. This article focuses on various non-cancerous lesions that are found in intra-abdominal fat and can be visualized by ultrasonography (US). This group includes:

  1. Visceral adiposity. Overdeveloped visceral adipose tissue is one of the causes of severe lifestyle diseases, such as metabolic syndrome, cardiovascular diseases and neoplasms(14). Despite this, visceral adiposity is ignored in a considerable majority of US scans, which should be considered an error. Informing patients about these lesions should mainly entail pro-health lifestyle changes thus contributing to the reduction of the risk of the diseases mentioned above and their complications. There have been numerous studies that aimed to determine the relationship between the distribution of intra-abdominal fat and its negative influence on a range of organs. It turned out that mesenteric fat has the greatest hepatogenic and aterogenic action. It releases multiple lipotoxic substances, such as free fatty acids, adiponectin, tumor necrosis factor (TNF-alpha), plasminogen activator inhibitor type 1 and others, directly to the portal circulation(411). That is why the most valuable information is not delivered by a US examination of the thickness of subcutaneous and extraperitoneal fat but rather that of the mesentery. This has been demonstrated in various studies which helped determine that this parameter is an independent risk indicator of severe diseases(5, 711). Liu et al.(12), based on a multivariate logistic regression analysis, demonstrated that the value that differentiates normal and thickened mesenteric folds is 10 mm. The odds ratio of metabolic syndrome increased by 1.35-fold for every 1-mm increase in the thickness of this structure over the value of 10 mm. Ultrasound is the only imaging modality enabling accurate visualization of mesenteric folds. This is preferably performed by applying the transducer slightly to the left and downwards from the navel (Fig. 1). The mean value of three thickest folds should be calculated. The examination is simple and provides clinically significant information since cardiovascular diseases, metabolic syndrome and neoplasms are threats for the contemporary population. If mesenteric folds cannot be visualized, one should measure the thickness of the mesenteric root located above the navel (according to our initial conclusions, the value exceeding 25 mm is of a similar relevance as fold thickness) (Fig. 2). Also, it must be emphasized that excessively developed visceral fat is not always associated with obesity. Normal body mass index (BMI) is noted in some patients(13), which additionally increases the relevance of mesentery evaluation in ultrasound imaging, and not only based on anthropometric parameters.

  2. Inflammatory lesions in the mesentery of the small intestine are rarer (0.6–3.42% of patients in abdominal computed tomography scans(14, 15)). Histology mainly distinguishes between sclerosing and retractile mesenteritis. Some authors supplement this division with lipodystrophy, the major part of which is fat necrosis rather than inflammation and fibrosis(16). The etiology of the disease is unclear. Various pathogenetic factors are enumerated: from autoimmune disorders to cancer-related reactions or injuries. Recently, scle-rosing mesenteritis has been observed to be a manifestation of sclerosing lesions associated with IgG4 infiltrates(17, 18). In most cases, the course of the disease is subclinical and selflimiting. The most alarming signs and symptoms include pain and palpable resistance. In rare cases, the disease has an acute onset and requires a surgical intervention due to intestinal ischemia(15, 19, 20). The sonographic symptomatology of sclerosing mesenteritis includes:

    • tumor-like thickening, usually of the small intestinal mesenteric root, with homogeneous, enhanced echogenicity (hyperechoic “sandwich sign”);

    • more rarely: a tumor-like mass with homogeneous, lower echogenicity;

    • poorly circumscribed margins;

    • the mass separates intestinal loops;

    • the superior mesenteric vessels do not show features of relocation or deformation;

    • lower compressibility of the mesentery upon transducer compression;

    • high arterial resistance index (RI) of 0.89–0.99 (Fig. 3 A, B).

    Retractile mesenteritis is manifested by a heterogeneous mass with areas of lower echogenicity(21, 22). These lesions are usually solitary masses (58/84), sometimes multiple lesions (15/84) and most rarely in the generalized form (11/84). It must be also remembered that apart from the most common small intestinal mesentery involvement, a similar process can also occur in the mesentery of the colon (mainly the sigmoid colon), greater omentum, retroperitoneal space and pelvis(23). The differential diagnosis should include various diseases: lymphoma, liposarcoma, rhabdomyosarcoma, lipoma, carcinoid, fibromatosis, mesenteric inflammatory reaction in the course of pancreatitis, mesenteric edema of various etiologies and visceral adiposity mentioned above(15, 2123).

  3. In approximately 90% of cases, the site of primary infarction (torsion) of the greater omentum is the right side. It can result from the following predisposing factors: structural anomalies in the omentum and its veins (particularly of the right side), thrombophilia, circulatory insufficiency and vasculitis as well as obesity, cough, excessive physical exertion and an abrupt change of the position of the torso. The secondary nature of this pathology is a consequence of an abdominal surgery, trauma, inflammation, presence of a cyst and abdominal hernia. In these cases, lesions can be located at various sites in the abdominal cavity(24, 25). A typical ultrasound image of omental infarction is characterized by: a slightly or moderately hyperechoic plaque-like mass greater than 5 cm (in adults) located under the abdominal integuments to the right of the navel. The mass is sensitive to compression but with no visible compressibility (Fig. 4 A). It shows no blood flow in an examination with colored blood flow mapping (Fig. 4 B). However, vessels on the periphery of a central hypoechoic necrotic area have been observed in children with this pathology. Sometimes, the lesion is surrounded with a hypoechoic rim, or slight amounts of fluid are found in the vicinity. Moreover, the medial aspect of the affected omentum adheres to the ascending colon which does not usually show wall thickening. The situation, particularly as far as vessels are concerned, is presented in a better way in a contrast-enhanced CT scan(2428). Because infarction of the greater omentum clinically resembles appendicitis, its assessment is very important from the point of view of adequate patient management since the thickened omentum can at times conceal an underlying pathology. In the considerable majority of cases, omental infarction resolves spontaneously without specific treatment. The lesion undergoes involution, mainly with fibrosis, sometimes with calcifications or adhesions between adjacent tissues. At times, a necrotic fragment detaches to the peritoneal cavity and behaves as a loose body. Occasionally, an abscess forms in consequence of omental infarction(29).

  4. Infarction of the lesser omentum is extremely rare. It is therefore a challenge for an ultrasonographer. The clinical picture of this pathology, including its spontaneous resolution, resembles infarction of the greater omentum. The only difference is the site, i.e. the position of a lesion between the left liver lobe, pancreas and stomach. The pathological mass gives a similar US image to that of necrotic fat tissue at other abdominal sites. It is hyperechoic, non-vascularized, sensitive and shows no compressibility(24) (Fig. 5 A–C). It can be mistaken for an exophytic tumor of the pancreas(30).

  5. Epiploic appendagitis (torsion) accounts for 1.3% of patients presenting with abdominal pain and constitutes 8.8 cases per million a year in the general population(31). These lesions are particularly common in the descending and sigmoid colon. That is why they can clinically resemble colonic diverticulitis. The former pathology is much more difficult to distinguish in ultrasound. Despite its superficial location under the abdominal wall, it does not distinguish itself clearly from adjacent tissues. An indicating sign is localized pain reported by patients or evoked with the use of a transducer. At this site, one can see a slightly hyperechoic structure, usually of ovoid shape and sometimes surrounded with a halo. It does not present vascularity or undergo deformation upon compression (Fig. 6 A, B). In some cases, a central hypoechoic area with a blurred outline can be spotted. Such a lesion sometimes adheres to the parietal peritoneum during deep inspiration. It usually slightly deviates externally and lies on the intestinal wall that is not thickened(24, 25, 32, 33). Elastography and contrast-enhanced ultrasound can be helpful in the diagnosis(33, 34). Lesions located deeper in the pelvis minor are usually imaged by transrectal ultrasound(35). There are cases in which omental infarction is indistinguishable from twisted epiploic appendage in US imaging. That is why van Breda Vriesman et al.(36) have proposed that such lesions be referred to as intra-abdominal focal fat infarction (IFFI). In all IFFI cases, it should be verified that the lesion is not a secondary fat pad as a reaction to inflammation, e.g. appendicitis or diverticulitis. This is indicated by blood flow within this structure seen in a color Doppler examination (Fig. 7)(32, 33). Moreover, primary epiploic appendagitis may mimic peritoneal implants of cancers, particularly ovarian carcinoma(37) (Fig. 8). Finally, it must be added that exceptional cases include torsion of the epiploic appendage of the hepatic ligamentum teres(24) or its detachment as a loose body into the peritoneum(38).

  6. Encapsulated fat necrosis mainly concerns patients after abdominal surgery and is rarely reported(25, 39). It can mimic liposarcoma, but it is well-circumscribed and does not invade adjacent tissues. Moreover, check-ups reveal a tendency to volume reduction and, sometimes, calcification (Fig. 9).

  7. Fat necrosis is frequently associated with pancreatitis and may mimic a neoplastic spread (Fig. 10). Clinical history and gradual regression of lesions, which are frequently calcified, are important(25).

  8. Swollen and hyperechoic fat tissue is often an evident sign of a lesion. It usually means that a pathological process spreads to adjacent structures. This indirect sign is frequently observed in appendicitis (in 98%) and diverticulitis (in 100%)(40), but also in Crohn's disease(41)(Fig. 11). This image is created by the thickened greater omentum and/or mesentery as well as reactive tissues which can constitute an obstacle for the visualization of an underlying pathological lesion. That is why computed tomography should be conducted if such a situation cannot be explained based on ultrasound imaging(40, 42, 43). A similar reaction can be seen in the lesser omentum in various pathologies of the epigastric region: stomach or duodenal ulcers, pancreatitis, hepatitis, cholecystitis, portal hypertension and cancers (mainly of the stomach and pancreas)(44)(Fig. 12).

  9. Intestinal malrotation is a congenital anomaly usually diagnosed in young children. During normal pregnancy, the intestines rotate by 270° counterclockwise. For practical purposes, this anomaly can be divided into three types(4547):

    • complete nonrotation is the most common defect. The small intestine occupies the right side of the abdominal cavity, and the large bowel is located on the left side. This is reflected in the position of the superior mesenteric vessels. Their interposition in a transverse view of the root of the small intestinal mesentery is manifested by the fact that the superior mesenteric artery is located on the right side and the synonymous vein is on the left (Fig. 13). However, this sign is not characterized by a high specificity since incomplete rotation has been observed with the vein located above the artery or without mesenteric vein transposition. This has been explained either with a pathological compression of the mesenteric root by a mass or reverse visceral position(48). According to our observations, scoliosis can be another cause. Since, in this anomaly, the mesenteric root is narrow, it sometimes twists around the axis made by the superior mesenteric artery, which is clinically manifested by signs of high gastrointestinal obstruction and in ultrasound – by its pathognomonic sign, i.e. whirlpool sign (Fig. 14 A, B). Internal paraduodenal hernia is another complication of this anomaly;

    • incomplete rotation with a broad spectrum of variants is characterized by a high position of the cecum, directly under the pyloric part of the stomach. This is frequently associated with the presence of a fibrous band of the peritoneum (band of Ladd) which intersects the duodenum and contributes to its obstruction;

    • reversed rotation is the rarest type of this anomaly. Its typical features include: the duodenum located anteriorly in relation to the superior mesenteric artery and the transverse colon running under this vessel(4547).

Fig. 1

A single view presents three fatty folds of the mesentery, with their thickness

JoU-2016-0004-g001.jpg
Fig. 2

Two views show fatty root of the small intestinal mesentery with visible superior mesenteric vessels

JoU-2016-0004-g002.jpg
Fig. 3

A. Two views show the small intestinal mesentery affected by sclerosing inflammation (arrows). B. The same mesenteric root presented in a CT axial image. Arrows mark the area of increased fat density

JoU-2016-0004-g003.jpg
Fig. 4

A. The transverse view of the right lumbar region presents infarction of the greater omentum (arrows). B. The same axis as in Fig. 4 A. Color Doppler set to detect slow flows does not show any vascularity

JoU-2016-0004-g004.jpg
Fig. 5

A. Two views show infarction of the lesser omentum (arrows). B. The same infarction in a computed tomography scan (arrows). C. Follow-up US examination 3 months after infarction of the lesser omentum (Fig. 5 A) shows almost normal thickness of the omentum (arrows). L – liver

JoU-2016-0004-g005.jpg
Fig. 6

A. Rare location of epiploic appendagitis on the transverse colon (A) in the vicinity of the gall bladder (GB). B. The same case in a computed tomography scan (arrows).

JoU-2016-0004-g006.jpg
Fig. 7

Secondary epiploic appendagitis (arrows) as a reaction in typhlitis

JoU-2016-0004-g007.jpg
Fig. 8

Ovarian carcinoma metastasis (M) mimics secondary epiploic appendagitis

JoU-2016-0004-g008.jpg
Fig. 9

Peripherally calcified necrosis (N) in the mesenteric root

JoU-2016-0004-g009.jpg
Fig. 10

Balser fatty necrosis (arrows) in the course of acute pancreatitis in two views

JoU-2016-0004-g010.jpg
Fig. 11

Evident hyperechoic reaction of the intestinal fat to 20-yearlong Crohn's disease. I – affected ileum

JoU-2016-0004-g011.jpg
Fig. 12

Arrows point to the thickened lesser omentum in a patient with gastric carcinoma. S – stomach, L – liver

JoU-2016-0004-g012.jpg
Fig. 13

Incomplete intestinal rotation in a 32-year-old male. SMA – superior mesenteric artery, SMV – superior mesenteric vein, ICV – inferior vena cava, GB – gall bladder

JoU-2016-0004-g013.jpg
Fig. 14

A. Transverse view of small intestinal mesenteric volvulus in the B-mode (arrows) in a 6-year-old girl. A – aorta, V – inferior vena cava. B. The same girl as in Fig. 14 A but in the duplex Doppler. The measuring gate is in the superior mesenteric artery which is the rotation axis; this caused mesenteric vein dilatation

JoU-2016-0004-g014.jpg

In this review, the authors have intentionally omitted other lesions located in the intra-abdominal fat, such as: vascular anomalies, collaterals associated with developed collateral circulation in the course of portal hypertension, cysts of various origin, post-traumatic lesions and other pathologies(24, 25, 47), since the volume of the paper, as specified in the rules and regulations of the Journal, does not allow them to be included.

Conflict of interest

Authors do not report any financial or personal connections with other persons or organizations, which might negatively affect the contents of this publication and/or claim authorship rights to this publication.

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  39. Yang DM,Kim HC,Kim SW,Choi SI,Dropped omental fat post laparoscopy-assisted distal gastrectomy with omentectomy mistaken for malignant peritoneal seeding on sonography J Clin Ultrasound 2014 42 305 307
    [PUBMED] [CROSSREF]
  40. Lee MW,Kim YJ,Jeon HJ,Park SW,Jung SI,Yi JG,Sonography of acute right lower quadrant pain: importance of increased intraabdominal fat echo AJR Am J Roentgenol 2009 192 174 179
    [PUBMED] [CROSSREF]
  41. Drouet M,Dubuquoy L,Desreumaux P,Bertin B,Visceral fat and gut inflammation Nutrition 2012 28 113 117
    [PUBMED] [CROSSREF]
  42. Noguchi T,Yoshimitsu K,Yoshida M,Periappendiceal hyperechoic structure on sonography J Ultrasound Med 2005 24 323 327
    [PUBMED] [CROSSREF]
  43. Kouamé N,N'goan-Domoua AM,N'dri KJ,Konan AN,Yao-Bathaix MF,N'gbesso RD,The diagnostic value of indirect ultrasound signs during acute adult appendicitis Diag Interv Imaging 2012 93 e24 28
    [CROSSREF]
  44. Smereczyński A,Sieć mniejsza jako wskaźnik patologii nadbrzusza Pol Przegl Radiol 1991 55 17 19
  45. Yeh WC,Wang HP,Chen C,Wang HH,Wu MS,Lin JT,Preoperative sonographic diagnosis of midgut malrotation with volvulus in adults: the „whirlpool” sign J Clin Ultrasound 1999 27 279 283
    [PUBMED] [CROSSREF]
  46. Pickhardt PJ,Bhalla S,Intestinal malrotation in adolescents and adults: spectrum of clinical and imaging features AJR Am J Roentgenol 2002 179 1429 1435
    [PUBMED] [CROSSREF]
  47. Okino Y,Kiyosue H,Mori H,Komatsu E,Matsumoto S,Yamada Y,Root of the small-bowel mesentery: correlative anatomy and CT features of pathologic conditions Radiographics 2001 21 1475 1490
    [PUBMED] [CROSSREF]
  48. Van Winckel M,Voet D,Robberecht E,„Whirlpool sign”: not always associated with volvulus in intestinal malrotation J Clin Ultrasound 1996 24 367 370
    [PUBMED] [CROSSREF]
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FIGURES & TABLES

Fig. 1

A single view presents three fatty folds of the mesentery, with their thickness

Full Size   |   Slide (.pptx)

Fig. 2

Two views show fatty root of the small intestinal mesentery with visible superior mesenteric vessels

Full Size   |   Slide (.pptx)

Fig. 3

A. Two views show the small intestinal mesentery affected by sclerosing inflammation (arrows). B. The same mesenteric root presented in a CT axial image. Arrows mark the area of increased fat density

Full Size   |   Slide (.pptx)

Fig. 4

A. The transverse view of the right lumbar region presents infarction of the greater omentum (arrows). B. The same axis as in Fig. 4 A. Color Doppler set to detect slow flows does not show any vascularity

Full Size   |   Slide (.pptx)

Fig. 5

A. Two views show infarction of the lesser omentum (arrows). B. The same infarction in a computed tomography scan (arrows). C. Follow-up US examination 3 months after infarction of the lesser omentum (Fig. 5 A) shows almost normal thickness of the omentum (arrows). L – liver

Full Size   |   Slide (.pptx)

Fig. 6

A. Rare location of epiploic appendagitis on the transverse colon (A) in the vicinity of the gall bladder (GB). B. The same case in a computed tomography scan (arrows).

Full Size   |   Slide (.pptx)

Fig. 7

Secondary epiploic appendagitis (arrows) as a reaction in typhlitis

Full Size   |   Slide (.pptx)

Fig. 8

Ovarian carcinoma metastasis (M) mimics secondary epiploic appendagitis

Full Size   |   Slide (.pptx)

Fig. 9

Peripherally calcified necrosis (N) in the mesenteric root

Full Size   |   Slide (.pptx)

Fig. 10

Balser fatty necrosis (arrows) in the course of acute pancreatitis in two views

Full Size   |   Slide (.pptx)

Fig. 11

Evident hyperechoic reaction of the intestinal fat to 20-yearlong Crohn's disease. I – affected ileum

Full Size   |   Slide (.pptx)

Fig. 12

Arrows point to the thickened lesser omentum in a patient with gastric carcinoma. S – stomach, L – liver

Full Size   |   Slide (.pptx)

Fig. 13

Incomplete intestinal rotation in a 32-year-old male. SMA – superior mesenteric artery, SMV – superior mesenteric vein, ICV – inferior vena cava, GB – gall bladder

Full Size   |   Slide (.pptx)

Fig. 14

A. Transverse view of small intestinal mesenteric volvulus in the B-mode (arrows) in a 6-year-old girl. A – aorta, V – inferior vena cava. B. The same girl as in Fig. 14 A but in the duplex Doppler. The measuring gate is in the superior mesenteric artery which is the rotation axis; this caused mesenteric vein dilatation

Full Size   |   Slide (.pptx)

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  40. Lee MW,Kim YJ,Jeon HJ,Park SW,Jung SI,Yi JG,Sonography of acute right lower quadrant pain: importance of increased intraabdominal fat echo AJR Am J Roentgenol 2009 192 174 179
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  41. Drouet M,Dubuquoy L,Desreumaux P,Bertin B,Visceral fat and gut inflammation Nutrition 2012 28 113 117
    [PUBMED] [CROSSREF]
  42. Noguchi T,Yoshimitsu K,Yoshida M,Periappendiceal hyperechoic structure on sonography J Ultrasound Med 2005 24 323 327
    [PUBMED] [CROSSREF]
  43. Kouamé N,N'goan-Domoua AM,N'dri KJ,Konan AN,Yao-Bathaix MF,N'gbesso RD,The diagnostic value of indirect ultrasound signs during acute adult appendicitis Diag Interv Imaging 2012 93 e24 28
    [CROSSREF]
  44. Smereczyński A,Sieć mniejsza jako wskaźnik patologii nadbrzusza Pol Przegl Radiol 1991 55 17 19
  45. Yeh WC,Wang HP,Chen C,Wang HH,Wu MS,Lin JT,Preoperative sonographic diagnosis of midgut malrotation with volvulus in adults: the „whirlpool” sign J Clin Ultrasound 1999 27 279 283
    [PUBMED] [CROSSREF]
  46. Pickhardt PJ,Bhalla S,Intestinal malrotation in adolescents and adults: spectrum of clinical and imaging features AJR Am J Roentgenol 2002 179 1429 1435
    [PUBMED] [CROSSREF]
  47. Okino Y,Kiyosue H,Mori H,Komatsu E,Matsumoto S,Yamada Y,Root of the small-bowel mesentery: correlative anatomy and CT features of pathologic conditions Radiographics 2001 21 1475 1490
    [PUBMED] [CROSSREF]
  48. Van Winckel M,Voet D,Robberecht E,„Whirlpool sign”: not always associated with volvulus in intestinal malrotation J Clin Ultrasound 1996 24 367 370
    [PUBMED] [CROSSREF]

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