Intra-abdominal fat. Part III. Neoplasms lesions of the adipose tissue

Abstract

This article focuses on various cancerous lesions that are found beyond organs in the intra-abdominal fat and can be visualized with ultrasonography. These lesions are divided into five groups. The first group includes primary benign tumors containing adipocytes, such as lipoma, lipoblastoma, hibernoma and other lesions with an adipose tissue component, such as myolipoma, angiomyolipoma, myelolipoma and teratoma. The second group comprises primary malignant adipocytecontaining tumors, including liposarcoma and immature teratoma. The third group contains primary benign tumors without an adipocyte component that are located in intra-abdominal fat. This is a numerous group of lesions represented by cystic and solid tumors. The fourth group encompasses primary malignant tumors without an adipocyte component that are located in intra-abdominal fat. These are rare lesions associated mainly with sarcomas: fibrosarcoma, malignant fibrous histiocytoma, hemangiopericytoma and leiomyosarcoma. An epithelioid tumor at this site is mesothelioma. The last but not least group includes secondary malignant tumors without an adipocyte component located in intra-abdominal fat. This is the most numerous group with prevailing carcinoma foci. For each of these groups, the authors present ultrasound features of individual lesions and discuss their differential diagnosis. In the vast majority of cases, the material for cytological and histological analysis can be obtained during ultrasound-guided procedures. This is the advantage of this imaging modality.

Ultrasound imaging of fat-containing structures located beyond organs is underestimated despite the fact that such structures can represent various pathologies, also neoplasms. Neoplastic tumors can be divided into primary and secondary. Primary mesenchymal tumors include benign and malignant lesions. It must be remembered that fatty structures, such as both omenta and the mesentery, contain not only adipose tissue components but also various proportions of connective tissue, blood and lymphatic vessels as well as nerves coated by the peritoneum. That is why the histogenesis of lesions appearing in this area can vary.

Primary benign adipocyte-containing tumors located in intra-abdominal fat

1. Lipoma is a rare tumor but can be found at various sites in the abdominal cavity (Fig. 1). Proliferating adipocytes are encapsulated. In US, the lesion is homogeneous, usually slightly hyperechoic with smooth outlines. Sometimes, individual lobules are separated from one another by thin fibrous septa. Color Doppler shows no signs of flow^(1–4). At times, this tumor can be encountered in a multiple form⁽⁵⁾ (Fig. 2). If it is of a large size, it can compress adjacent tissues or organs and become heterogeneous. In such cases, imaging is incapable of distinguishing it from liposarcoma⁽¹⁾.

2. Lipoblastoma is a type of a benign tumor with embryonic fat. It is mainly encountered in children. It is usually found in the extremities and torso whereas abdominal cavity belongs to its rather rare sites^{(6, 7)}. In US, such tumors are echogenic. They may sometimes contain cysts or hypoechoic foci. Lipoblastomatosis is a form of this tumor characterized by aggressive localized growth⁽⁷⁾.

3. Hibernoma is a benign tumor, mainly composed of brown fat, in whose cells the numbers of mitochondria responsible for enhanced metabolic activity are impressive. These tumors are rarely encountered in the retroperitoneal space but are also echogenic with well-or ill-defined margins. Their characteristic feature is evident flow in color Doppler⁽⁷⁾.

4. Other benign tumors with a fat component, such as myolipoma, angiomyolipoma and myelolipoma, apart from teratoma (which is usually benign), tend to be homogeneous with echogenicity increased to various degrees (Fig. 3, 4). Adrenal adenoma, which contains lipids and is hypoechoic, is an exception. Only gonadal germ cell tumors, such as teratoma and dermoid cyst that arise from several germ layers, frequently have irregular echotexture due to the presence of fluid sebum, hair, soft tissues and bony elements. That is why they are encountered in solid, cystic or solid-cystic forms (Fig. 5)^(7–14). Mature fat tissue can also be found in choristoma which, however, is not a neoplasm. All of the aforementioned tumors usually grow to large sizes before causing clinical symptoms. They can produce the mass effect but do not infiltrate adjacent tissues. These lesions are usually found in the retroperitoneal space^(12–14).

Fig. 1.

Two views show lipoma (arrows) as a slightly echogenic lesion in the supraperitoneal fat

Fig. 2.

Three lipomas (L) in the small bowel mesentery, which in computed tomography showed density ranging from –57 to –74 Hounsfield units

Fig. 3.

Two views show angiomyolipoma (L) located entirely in the adipose capsule of the right kidney. An arrow points to the site of regrowth in the form of the beak sign

Fig. 4.

Myelolipoma in the right suprarenal field (arrow) as a visible hyperechoic mass

Fig. 5.

A heterogeneous mass arising from the retroperitoneal space is a mature teratoma with slight calcifications (arrows)

Liposarcoma

Liposarcoma is the only malignancy deriving from adipose tissue that is relatively frequently encountered in the retroperitoneal space (it constitutes nearly 1/3 of sarcomas at this site and 10–15% of all neoplasms of this type)^{(7, 15–17)}. According to the WHO, these tumors can be divided into five histological subtypes depending on the grade of their differentiation (well-differentiated, dedifferentiated, myxoid, round cell, pleomorphic), which is relevant in prognosis^{(7, 15)}. Well-differentiated liposarcoma is difficult to distinguish morphologically from lipoma. Its presence can be indicated only by uneven margins and heterogeneous enhancement upon contrast agent administration^{(1, 7)}. Poorly differentiated subtypes account for even 40% of local relapses, and metastases are observed in 17% of cases⁽¹⁵⁾. As has already been mentioned, well-differentiated liposarcoma is difficult to distinguish from lipoma also in sonography. One of the differential criteria can be tumor's reaction to compression with a transducer (Fig. 6). More aggressive forms of this tumor, however, tend to be unevenly delineated, present heterogeneous echotexture and infiltrate adjacent tissues (Fig. 7). Pathological blood flow can be observed in certain parts of the tumor (Fig. 8). Myxoid liposarcoma is characterized by a cystic structure and should be distinguished e.g. from lymphangioma, teratoma or cystic mesothelioma.

Fig. 6.

Relapse of liposarcoma in the small bowel mesentery. No lesion compressibility when pressure is applied with the transducer (arrow)

Fig. 7.

Heterogeneous retroperitoneal liposarcoma infiltrates into adjacent tissues (arrows)

Fig. 8.

Mesenteric liposarcoma with pathological vascularity

Finally, immature teratoma must be mentioned. It is a primary germinal tumor that can contain adipose tissue and occurs at similar sites. Compared with mature teratomas, such tumors are encountered significantly more rarely. Moreover, they are characterized by the predominance of a solid component, and the only sign suggesting a malignancy is poorly circumscribed margins. A chance for malignant transformation is observed in approximately 25% of such tumors, mainly in glial tissue^{(7, 12)}.

Primary benign tumors without an adipocyte component located in intra-abdominal fat

These tissues include numerous pathologies of diversified morphology. Cystic lesions can correspond to mesenteric cysts, lymphatic or vascular angiomatosis and even a cystic form of peritoneal mesothelioma, which is considered a benign lesion (Fig. 9)^{(1, 18–23)}. The differential diagnosis of these pathologies should include ovarian cystic tumors, endometrial cysts and cystic tumors growing beyond organs, e.g. of the pancreas, kidneys or liver. Solid tumors found at these sites include: leiomyoma and rhabdomyoma, angiomas as well as stromal, neurogenic and desmoid tumors (Fig. 10)^{(1, 16, 24, 25)}. Desmoid tumors, also called fibromatosis, are an interesting group of benign tumors that exhibit local aggressiveness and have considerable tendency to recur (in approximately 50% of cases)^{(25, 26)}. Wang et al. have analyzed ultrasound presentation of 44 such tumors⁽²⁶⁾. All lesions were hypoechoic with slightly irregular echo patterns, 59% of cases were well-defined and 41% had irregular margins. Most lesions showed no flow in the color Doppler scan (66%). Moderate flow was detected in 23% and marked flow – in 11%. Infiltration into adjacent tissues was found in 48% of lesions (Fig. 11). The differential diagnosis should include sarcomas, mainly the two types that are most frequently found in soft tissues: histiocytic fibrosarcoma and liposarcoma, i.e. lesions characterized by higher echogenicity^{(25, 26)}. It is of note that desmoid tumors frequently coexist with familial adenomatous polyposis, which is estimated at 9–18% of cases⁽²⁷⁾. Of all imaging modalities, magnetic resonance imaging is the most specific in diagnosing fibromatosis^{(25, 27)}. Some authors recommend punch or even surgical biopsy in the event of doubts. In this case, sensitivity and specificity exceed 90%^{(14, 25, 26, 28)}.

Fig. 9.

Mesenteric lymphangioma as a multilocular lesion without flow (arrow)

Fig. 10.

Retroperitoneal neuroblastoma in a 13-year-old (arrows). A – aorta, V – inferior vena cava

Fig. 11.

Desmoid, poorly vascularized tumor (D) in the small bowel mesentery

Primary malignant tumors without an adipocyte component located in intra-abdominal fat

These changes are rarely encountered but they represent a rich spectrum of mainly mesenchymal neoplasms: fibrosarcoma, malignant fibrous histiocytoma, hemangiopericytoma, leiomyosarcoma, rhabdomyosarcoma and gastrointestinal stromal tumors^{(1, 16, 29)} (Fig. 12). Small tumors are usually homogeneous. Larger lesions show polycyclic and blurred margins, and their structure is heterogeneous. They also quite frequently infiltrate into adjacent tissues and organs. An epithelioid malignant neoplasm encountered at this site is malignant peritoneal mesothelioma, a lesion that almost exclusively develops in males in the fifth and sixth decade of life. It can assume two morphological forms: irregular peritoneal infiltration without ascites (dry appearance) (Fig. 13) and nodular thickening of the peritoneum and greater omentum with ascites (wet appearance)⁽²²⁾. Lesions of this type must be distinguished from papillary serous carcinoma of the peritoneum (a rare neoplasm found in elderly women), abdominal carcinomatosis, in which ascites prevails over implants, and peritoneal tuberculosis, in which there are no tumorous lesions (but ascites is present, the greater omentum is thickened with preserved smooth surface and the mesenteric lymph nodes are enlarged). Lymphomas, however, are characterized by considerable abdominal lymphadenopathy, rare and slight ascites and no omental involvement.

Fig. 12.

Rhabdomyosarcoma with rich vascularity in the retroperitoneal space (arrows)

Fig. 13.

Two views present poorly vascularized malignant mesothelioma of the greater omentum (M)

Secondary malignant tumors without an adipocyte component located in intra-abdominal fat

This is the most numerous group with prevailing carcinoma foci, mainly deriving from abdominal organs, such as pancreas, stomach, large bowel or ovaries. These lesions spread by direct extension, via the lymphatic system or blood stream and through the peritoneal cavity. Their echotexture can vary. Hypoechoic foci with the solid-cystic structure (Fig. 14) and thickened parietal peritoneum (its normal thickness is up to 1.5 mm) (Fig. 15) are the easiest to detect. Echogenic lesions that only slightly differ from the surrounding tissues are the hardest to find (Fig. 16). Peritoneal sites at which carcinoma implants tend to develop are: the recto-uterine pouch, right iliac fossa, right paracolic gutter and the region of the upper sigmoid mesentery. Moreover, ovarian carcinoma cells frequently migrate to the supra- and subhepatic area (Fig. 17)^{(1, 16)}. Well-designed prospective studies have proven ultrasound imaging to be highly useful in detecting abdominal carcinomatosis^{(30, 31)}. It occurred that lesions in the greater omentum were the easiest to detect (91%) whereas those in the small bowel mesentery were the hardest to find (67%). Moreover, ultrasound guidance enables one to obtain diagnostically valuable material for cytological and histological analysis in the vast majority of such cases^(31–33).

Fig. 14.

Metastasis of malignant melanoma (M) from the interscapular space to the small bowel mesentery

Fig. 15.

Peritoneal carcinomatosis of ovarian carcinoma. Thickened hypoechoic parietal peritoneum with signs of vascular flow (arrows)

Fig. 16.

Two views show a hyperechoic implant of ovarian carcinoma in the gastrocolonic ligament (arrows)

Fig. 17.

Ovarian carcinoma implants in the pouch of Morison (arrows)

Another rare neoplasm encountered in fatty bodies of the abdominal cavity is non-Hodgkin lymphoma^{(1, 16, 29, 34)}. The involvement of the small bowel mesentery, with prominent, large mesenteric lymph nodes, is observed to occur in a half of patients with this neoplasm⁽¹⁾. These lymph nodes, together with the superior mesenteric vessels, create a so-called “sandwich” image (Fig. 18)⁽³⁵⁾. An extranodal infiltration is a rarer manifestation of this pathology (Fig. 19). Finally, carcinoid must be mentioned. It is usually a small neuroendocrine neoplasm located in the small bowel. Sometimes, the first morphological sign of its existence is the presence of mesenteric abnormalities in the form of enlarged lymph nodes or a hypoechoic mass. Mesenteric thickening or contraction, which can lead to small bowel obstruction, is more rarely a predominant element of the image^{(36, 37)}. Any doubts in the assessment of these lesions require verification in computed tomography and, sometimes, magnetic resonance imaging^{(7, 8, 10, 38, 39)}. Ultrasound imaging, however, enables precise, percutaneous sampling for cytological and histological analysis, which is worth remembering and applying.

Fig. 18.

“Sandwich” sign in the small bowel mesentery (arrows) created by enlarged lymph nodes surrounding the superior mesenteric vessels – a manifestation of non-Hodgkin lymphoma

Fig. 19.

Extranodal location of follicular lymphoma in the small bowel mesentery (arrow)

Lesions in the lymph nodes, which are relatively frequently affected by various neoplastic and non-neoplastic processes, have been presented only briefly since these issues are too broad to be included in this review.

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.