First published online October 12, 2006
British Journal of Radiology (2007) 80, 284-292
© 2007 British Institute of Radiology
doi: 10.1259/bjr/50066770
Metastatic carcinoma of the breast: the appearances of metastatic spread to the abdomen and pelvis as demonstrated by CT
M Brookes, BSc, MB BS, MRCP1,
D MacVicar, MA, FRCP, FRCR2 and
J Husband, OBE, FMedSci, FRCP, PRCR2
1 Department of Radiology, St George's Hospital, Blackshaw Road, London SW17 0QT, 2 Academic Department of Diagnostic Radiology, Royal Marsden NHS Foundation Trust, Downs Road, Sutton, Surrey SM2 5PT, UK
Correspondence: Dr David MacVicar, Royal Marsden NHS Foundation Trust, Downs Rd, Sutton, UK. E-mail: david.macvicar{at}rmh.nhs.uk
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Abstract
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This review illustrates some CT appearances of metastatic breast cancer in the subdiaphragmatic abdomen and pelvis. Such manifestations are not uncommon in advanced disease and familiarity will enable confident diagnosis in patients at risk for metastatic disease.
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Introduction
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It is well recognized that carcinoma of the breast can metastasize to any organ, although distant metastases are unusual at the time of diagnosis. Metastatic disease frequently arises between 2 years and 5 years following diagnosis. Its likelihood is influenced by factors such as regional nodal status at presentation and histological tumour grade. The most common sites of metastases, apart from regional lymph nodes, are lung, bone, liver and pleura [1]. CT may be used to demonstrate metastatic spread of disease to sites in the abdomen and pelvis when patients are imaged during disease follow up. The appearances of breast cancer metastases are varied, although they may conform to certain patterns in some organs. The pathological tumour type is thought to have a bearing on the sites of spread, with lobular carcinoma (as opposed to invasive ductal carcinoma) being more commonly associated with unusual sites including the gastrointestinal tract, genitourinary tract, uterus or adnexae [2]. This review aims to illustrate these appearances, and to emphasise the importance of scrutinizing infradiaphragmatic sites in order to accurately assess the stage of disease and response to treatment.
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Liver
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Liver metastases are present in up to 71% of cases as demonstrated by autopsy studies [3]. The typical appearance is of an irregular, ill-defined low attenuation area within the liver parenchyma, best imaged during the portal venous phase (Figure 1
) [4]. Most metastases are hypovascular when compared with the surrounding liver parenchyma and this accounts for the appearance of relatively low attenuation. The periphery of the lesion may show some contrast enhancement. In the presence of hepatic steatosis, some metastases may be of higher attenuation than the surrounding liver. Homogeneously hypervascular metastases are rare and arterial phase dominant CT has been demonstrated to be of no benefit [5]. The irregular shape of deposits, combined with volume averaging with some machines, explains the lack of a clear margin between a metastasis and normal parenchyma. Lesions less than 5–10 mm cannot be readily assessed by CT, or confidently differentiated from benign lesions such as simple hepatic cysts, as the spatial resolution and contrast resolution of CT is insufficient for lesions below this size [6].
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Figure 1. There are bulky low attenuation masses in the liver. They are centrally of low attenuation with some uptake of contrast at the periphery.
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In some cases diffuse infiltration of the liver with metastatic deposits can have very similar imaging appearances to cirrhosis (so-called "pseudocirrhosis"), and pose some problems in interpretation (Figure 2) [6, 7]. This phenomenon is particularly common in metastatic breast cancer and may be seen with untreated hepatic metastatic disease where a periportal fibrotic process may occur [7]. The liver may be of normal size with an irregular margin or even shrunken. Occasionally the presence of ascites causes further confusion. "Pseudocirrhosis" may also develop while the patient is on treatment for liver metastases. Hepatic steatosis can be a result of treatment with tamoxifen or cytotoxic chemotherapy, but the appearances of these phenomena are distinctive (Figures 3 and 4) [8].
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Figure 2. "Pseudocirrhosis" in a patient 3 years after diagnosis of breast cancer. (a) Contrast-enhanced CT demonstrates a non-enlarged liver with mixed attenuation nodules, irregular outline and ascites. (b) Ultrasound reveals diffusely echogenic pattern without obvious discrete masses. The appearance was entirely stable on imaging over an 8 month interval, at which time the clinician insisted on a biopsy which revealed metastatic breast cancer.
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Figure 3. CT of liver shows knobbly outline, diffuse nodularity and ascites. This pseudocirrhotic appearance is a fairly common manifestation of metastatic breast carcinoma.
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Figure 4. The background liver parenchyma has low attenuation as a result of diffuse fat infiltration. In addition there are several metastatic deposits that are seen as irregular masses of low attenuation, with a periphery that enhances avidly after the administration of intravenous contrast. Development of fatty change while on treatment can increase conspicuity of the enhancing rim simulating enlargement of lesions which are stable in size.
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Focal fatty change within the liver can be misinterpreted as metastatic disease, although the lack of mass effect and the absence of liver architecture distortion can help in their differentiation from secondary deposits. Focal fatty change is seen in typical sites, e.g. adjacent to the falciform ligament (Figure 5). If differentiation is still not possible then in-phase/opposed-phase T1 weighted gradient echo MRI can be used to clarify the likely aetiology of a suspicious lesion [9]. Simple hepatic cysts can occasionally cause problems in differentiation from metastatic deposits if they are less than 1 cm in length. When larger than 1 cm they are easily distinguishable by the presence of a well-defined margin and homogeneous contents of fluid attenuation.
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Figure 5. A small area of focal fatty change is seen in segment 4b of the liver, adjacent to the falciform ligament(arrow). The liver architecture is normal, and no other abnormalities were seen within the liver. This appearance should not be misinterpreted as metastatic disease.
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Spleen
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Although splenic metastases are present microscopically in up to 18% of cases at post-mortem examination [10], the incidence of macroscopically apparent disease is only 1–2%. Symptoms attributable to splenic metastases are rare, although pain as a result of splenomegaly is recognized. There are reported cases of immune thombocytopenic purpura as a result of diffuse metastatic infiltration of the spleen by breast carcinoma [11]. Splenic metastases can occur in isolation, and if there are no other sites of metastases, solitary splenic deposits may be treated by splenectomy [12]. The typical appearance of metastases is similar to the pattern of disease within the liver, with an area of irregular low attenuation that has no well-defined margin separating it from normal splenic parenchyma (Figure 6). Lesions can be multiple and diffusely infiltrative, sometimes causing splenic enlargement (Figure 7). Benign splenic cysts and focal fatty change are unusual within the spleen and rarely cause problems in characterizing low attenuation lesions within the spleen.
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Figure 6. There is a solitary round area of low attenuation within the spleen that was not present on earlier imaging and signifies a metastasis.
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Figure 7. The spleen is enlarged and contains numerous ill-defined metastases, which have similar characteristics to those within the liver.
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Adrenal glands
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The most common endocrine organ involved as a site of metastatic disease is the adrenal gland, although the thyroid and pituitary glands can be involved [13]. Metastatic infiltration is suggested by loss of the normal "Y" or inverted "V" configuration of the gland, or by an increase in size (Figure 8). If no previous imaging is available for comparison it can be difficult to differentiate between a metastasis and a benign adrenal adenoma. Certain criteria such as size and attenuation can aid differentiation, but the presence of bilateral lesions is unhelpful as bilateral adenomas occur with similar frequency to bilateral metastases in patients with a known primary neoplasm [14].
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Figure 8. A 25 mm x 15 mm metastasis is present in the right adrenal gland, distorting the normal morphology.
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The normal width of the adrenal gland body is 8 mm on the left, and 6 mm on the right as demonstrated by CT [15]. Therefore the size of the adrenal lesion can be a guide: in the absence of previous imaging as a means for comparison, lesions less than 3 cm in diameter are likely to be benign and greater than 5 cm likely to be malignant [16]. An attenuation of less than 10 HU on non-enhanced CT (NECT) has been shown to have a 100% sensitivity for benign adenomas (and specificity of 68%), although contrast-enhanced computed tomography (CECT) does not demonstrate such a clear threshold as to allow accurate discrimination [17]. Any new adrenal lesion arising during breast cancer follow up is likely to be metastatic. Metastases tend to be asymptomatic, but hypoadrenalism does occasionally occur, especially with bilateral adrenal involvement [18, 19]. A variety of "problem solving" techniques for adrenal nodules can be employed, including subsequent unenhanced CT, MRI or biopsy.
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Lymph nodes in the retroperitoneum and pelvis
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The preferential lymph drainage of the breast is to the axillary, transpectoral, supraclavicular and internal mammary nodes. Nodal involvement at more distant sites including the abdomen the and pelvis may occur in the absence of involvement of local or mediastinal groups. The radiologist needs to be alert to unusual sites of lymph node metastases when staging carcinoma of the breast. Furthermore, the upper normal value of short axis diameter for what constitutes lymphadenopathy varies from site to site, e.g. 6 mm for retrocrural nodes, 8 mm for upper para-aortic and retroperitoneum, 10 mm for portocaval space [20].
Normal abdominal and pelvic lymph nodes have uniform attenuation, or a low attenuation centre, reflecting the presence of central fat. The size, shape and number of nodes at a particular site can also help to decide whether abdominal or pelvic lymph nodes are infiltrated with metastases. The typical appearance of a nodal metastasis is of an enlarged node that has lost its normal oval morphology (Figures 9–11). Metastatic nodes from breast cancer can demonstrate central low attenuation, possibly representing necrosis or cystic change, but rarely demonstrate calcification, even after treatment.
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Figure 9. An enlarged retrocrural node measuring 9 mm in short axis is seen adjacent to the aorta (arrow) and represents a site of metastatic infiltration.
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Figure 10. There are several lymph nodes measuring up to 15 mm in the retroperitoneum that are encircling the aorta and inferior vena cava.
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Figure 11. Two discrete mesenteric nodes(arrow) are visible measuring up to 12 mm in short axis, in a patient with widely disseminated disease.
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In some cases discrete nodal enlargement is not identifiable on CT and diffuse infiltrative tissue is present. From imaging criteria it is not always clear whether this pattern of disease is truly nodal with perinodal malignant retroperitoneal fibrosis or a manifestation of an extranodal infiltrative process. It is sometimes associated with peritoneal involvement by metastatic disease and can present with hydronephrosis (Figure 12).
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Figure 12. There are no discrete nodal mass lesions but there is retroperitoneal fat stranding(arrow) which can indicate infiltration by metastatic breast cancer of retroperitoneal (and mediastinal) fat. Note also the left hydronephrosis as a result of malignant retroperitoneal fibrosis.
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In addition to ensuring that a review is made of all the lymph node groups within the abdomen and pelvis, the radiologist must be able to identify variants of normal anatomical structures that can simulate lymphadenopathy. An example is the communicating vein between the left renal vein and the left ascending lumbar vein, a variant that is visible in up to 20% of abdominal CT examinations and can be mistaken for para-aortic lymphadenopathy [21].
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Bone
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Although CT is not routinely used to assess the presence of bony metastases, they are often visible when imaging the abdomen or pelvis as the vertebrae and pelvis are the two most common sites for haematogenous spread to bone (62% and 59% of cases at post-mortem examination, respectively) [22]. This distribution reflects the drainage of the vertebral vein [23]. Metastases are sometimes asymptomatic (and often not visible on plain radiographs), but because of the high frequency of bony metastases in breast cancer a review of the skeleton on bone windows should be undertaken routinely and may also identify sites of potential complications such as pathological fracture or spinal cord compression. Pain can occur when the bony cortex is eroded sufficiently to cause a pathological fracture or when enough trabecular bone has been lost to cause collapse of a vertebral body (Figure 13). Metastases in the spine can extend beyond the bony cortex as a soft tissue mass, causing compression of the cord or nerve roots with consequent symptoms and signs (Figure 14).
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Figure 13. 3D CT sagittal reformat of lower thoracic and lumbar spine: sclerotic metastases are seen within the bodies of the T12 and L1 vertebrae. There is loss of height of the L1 vertebral body and posterior displacement of bone into the spinal canal.
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Figure 14. (a) Axial view at the level of L4 using soft tissue windows. A soft tissue mass (black arrow) is seen to arise from the posterior aspect of the vertebral body and is compressing the cauda equina. There is also a deposit in the right psoas (white arrow) causing asymmetry of the muscles. (b) Bone windows demonstrated a destructive metastasis affecting the vertebral body and posterior elements.
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Bony metastases have a lytic, sclerotic or mixed appearance, depending on how tumour cells influence surrounding bone and also on what treatment has been given (Figures 15 and 16). Malignant acute vertebral collapse (as opposed to "benign" vertebral collapse caused by osteoporosis) is characterized by cortical bone destruction of the vertebral bodies, destruction of cancellous bone, destruction of pedicles and posterior elements or the presence of a focal paraspinal soft tissue mass.
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Figure 15. A purely lytic metastasis has eroded the left pedicle of L1, but there is no associated soft tissue mass.
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Figure 16. A deposit causing sclerosis is seen within the vertebral body whilst the metastasis in the right iliac blade has eroded the bone with a lytic appearance.
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Although CT is not routinely used to further evaluate suspicious lesions detected by radionuclide scintigraphy, it has a role when imaging by MRI is not available or is contraindicated. Bone scintigraphy remains the investigation of choice to diagnose the presence of bone metastases in the first instance.
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Peritoneum
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The presence of metastatic deposits to the peritoneum is not uncommon, but is often difficult to recognize on CT. Transcoelomic spread to the peritoneal cavity can cause the development of malignant ascites, which allows further seeding to more distant sites, such as the pouch of Douglas, small bowel mesentery and greater omentum (Figure 17). A study of 260 abdominal CT examinations of patients with breast cancer demonstrated ascites in 5.4%, and peritoneal carcinomatosis in 2.6% [24].
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Figure 17. Diffuse, ill-defined nodularity and stranding is seen within the omental fat (arrows), a characteristic appearance of peritoneal deposits.
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Haematogenous spread of tumour emboli to the stomach or bowel serosa is another mechanism by which unusual sites in the abdomen and pelvis can demonstrate metastatic deposits [25]. Carcinoma of the breast (along with lung cancer and malignant melanoma) has a relatively high incidence of metastasis to the bowel and peritoneal reflections. On CT this can appear as thickening of bowel wall if there is serosal involvement or even cause bowel obstruction (Figure 18). Invasive lobular carcinoma is more likely than invasive ductal carcinoma to metastasize to the peritoneum (3.1% vs 0.6%) [26].
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Figure 18. In a patient with known metastatic breast cancer presenting with vomiting, a mass lesion in the duodenum is demonstrated(arrows). Endoscopy showed a mural mass and biopsy confirmed metastatic breast carcinoma.
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Genitourinary
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The renal tract is an unusual site for disease spread, with the kidney more often involved than the ureter or bladder [1]. The renal parenchyma can be a site for haematogenous spread, akin to the liver or spleen (Figure 19). If the ureter is involved then hydronephrosis of the ipsilateral kidney can develop as a result of urinary obstruction [27]. Although focal ureteric thickening can occasionally be seen on CT as a result of metastases, it is far more common to see consequent hydronephrosis. It is even more uncommon for the bladder to be involved, the appearance on CT being that of an irregularly thickened bladder wall (Figure 20).
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Figure 19. Several low attenuation metastases(black arrow) are seen in the cortex of both kidneys. They have no clear margins and are expansile. The attenuation is higher than that of fluid within the gallbladder and hence they are not simple renal cysts. Note also hepatic metastatic disease (white arrow). Hepatic lesions were of similar attenuation and morphology to renal deposits and a presumptive diagnosis was made from the imaging features.
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Figure 20. Bladder wall is irregularly thickened in this patient who had metastases in numerous other sites throughout the pelvis. Urine cytology was positive for the presence of malignant cells, metastatic from breast cancer.
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Metastases in the ovary or uterus are present in up to 21% of patients according to autopsy studies [13]. The incidence of detectable disease by CT imaging is significantly lower but still well recognized. An even smaller proportion of patients (<1%) will have metastases within the pelvis but at no other site [28]. The ovary is the most common pelvic organ to be affected (Figure 21), although the cervix and vagina are also recognized sites of disease spread [29]. There are a few reported instances of breast carcinoma metastases manifesting as post-menopausal bleeding when the endocervix is involved [30].
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Figure 21. A 4.5 cm adnexal mass, an ovarian deposit of breast cancer, with an irregular convex anterior border is seen to indent the posterior aspect of the bladder.
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Other sites
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Any organ can be involved in metastatic breast cancer, and hence there are innumerable ways that they can manifest on CT or other imaging modalities. Other recognized sites of tumour deposits include the pancreas [31], skin, subcutaneous tissues or muscle (Figures 14a
and 22). The consequence of metastatic spread may be more apparent than the soft tissue mass itself, for example hydronephrosis as a result of peritoneal disease or bowel obstruction as a result of extrinsic compression [32].
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Conclusion
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This pictorial review aims to illustrate that breast cancer can metastasize to any site, including to organs below the diaphragm. These are often visible when CT is used for staging or to monitor treatment response. The appearance of metastatic disease is diverse and correlation of suspicious findings with earlier imaging when available is often helpful. In our centre, investigation with CT is usually precipitated by clinical symptoms, signs or biochemical change. Where clinical suspicion of pelvic recurrence is high, the pelvic region is included, although this is not done in all cases. Because of the relatively high incidence of spread of disease to the abdomen and pelvis, adequate bowel preparation and use of oral contrast or water is recommended to help identify involved lymph nodes or peritoneal deposits. Use of intravenous contrast will help differentiate lymph nodes from adjacent vascular structures and aids detection of deposits to liver, spleen and kidneys. The histological subtype of the tumour is associated with different patterns of disease spread, with lobular carcinoma more commonly associated with unusual patterns of abdominal spread.
Received for publication April 26, 2005.
Revision received September 6, 2005.
Accepted for publication September 19, 2005.
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Abstract
Introduction
