Review
Women's Imaging
April 23, 2014

Distant Metastatic Disease Manifestations in Infiltrating Lobular Carcinoma of the Breast

Abstract

OBJECTIVE. This article reviews unusual distant metastatic patterns of infiltrating lobular carcinoma (ILC) of the breast.
CONCLUSION. ILC of the breast tends to spread to the gastrointestinal tract, genitourinary tract, peritoneum, retroperitoneum, and leptomeninges in addition to common visceral sites such as the liver, bone, and lung. Knowledge of these unusual metastatic manifestations and disease patterns may aid in differentiating distant metastatic disease from secondary primary cancers and help plan appropriate therapy.
Breast cancer is a histologically heterogeneous disease. Infiltrating ductal carcinoma (IDC) accounts for approximately 90% of breast cancers, whereas infiltrating lobular carcinoma (ILC), the second most common breast carcinoma, comprises approximately 10% of breast cancers [1, 2]. Although ILC accounts for only 10% of breast cancers, its incidence is twice that of invasive cervical cancer and equal to that of ovarian cancer and thus affects a large number of women [3]. The results of an epidemiologic study suggest that the incidence of ILC is increasing in postmenopausal women [4], possibly owing to hormone replacement therapy in this population.
The histopathologic appearance of ILC is different from that of IDC. ILC is characterized by small round cells that infiltrate the breast stroma in a single-file (“Indian-file”) pattern and encircle benign mammary ducts and lobules in a targetoid fashion [2, 5]. This type of infiltration through the breast parenchyma typically does not destroy anatomic structure or incite substantial connective tissue response. Because of this mode of infiltration, ILC often fails to form a distinct mass in the breast. Thus, the early detection of ILC by physical examination or mammography may be challenging, and locally advanced disease is not rare. In addition, ILC tends to have a multifocal, multicentric distribution and to occur in both breasts [611].
The distant metastatic pattern of ILC also differs significantly from that of IDC. Whereas IDC often metastasizes to the lung, liver, bone, and brain, ILC tends to spread to the gastrointestinal tract, genitourinary tract, peritoneum, retroperitoneum, and leptomeninges [2, 1216]. Approximately 3–10% of breast cancer patients have metastatic disease at their initial diagnosis; recurrent disease or metastasis occurs in approximately 30% of patients during follow-up after initial treatment [1720]. Some investigators have suggested that, compared with IDC, ILC has a higher distant metastasis rate [12, 13, 21], likely because of its infiltrative nature. It has been postulated that in ILC loss of E-cadherin, the cell-to-cell adhesion molecule, facilitates the metastasis process. Like ILC in the breast, metastatic ILC tends to infiltrate the affected organs in a diffuse process instead of forming a discrete tumor nodule.
Because radiologists play vital roles in the staging and surveillance of breast cancer patients, a familiarity with the pattern of distant ILC metastasis is essential to accurately interpret imaging study findings or to suggest a primary breast malignancy if the patient presents initially with distant metastases. However, reports describing the distant metastatic patterns of ILC are scarce in the radiology literature, and knowledge regarding ILC metastasis derives largely from autopsy and clinical series. Aside from a handful of case reports, only one large series describing the metastatic pattern of ILC on CT of the chest, abdomen, and pelvis in 57 patients has been published [15]. To our knowledge, no single report has provided a comprehensive description of ILC metastasis including the CNS and orbit. In this article, we review the available literature to illustrate ILC's unusual pattern of metastasis (Tables 1 and 2). This knowledge may help radiologists differentiate metastatic ILC from secondary site-specific primary tumors, which is crucial to treatment planning.
TABLE 1: Rates of Metastasis to Different Sites From Infiltrating Lobular Carcinoma (ILC) of the Breast Based on Clinical, Autopsy, and CT Findings
SitesRate of ILC Metastasis (%)
 Clinical Findings [2, 16]Autopsy Findings [12, 14]CT Findings [15]
Lungs or pleura3-921-4823-33
LeptomeningesNA29NA
Gynecologic organs2-536-5221
Gastrointestinal tract520-4332
Peritoneum or retroperitoneum360-9316-30
Distant lymph nodes3-1621-8047
Bone21-3560-6481
Liver6-743-6832

Note—NA = not available.

TABLE 2: Unusual Manifestations of Metastatic Infiltrating Lobular Carcinoma of the Breast
SitesImaging Findings
Gastrointestinal tractDiffuse infiltration of bowel wall of the stomach (linitis plastica) instead of mural masses
OvaryMixed cystic and solid masses (Krukenberg syndrome)
PeritoneumNumerous tiny nodules infiltrating peritoneum rather than large space-occupying peritoneal masses; “omental caking”
RetroperitoneumNumerous tiny nodules infiltrating retroperitoneal fat; infiltration or implants of ureters; hydronephrosis; retroperitoneal adenopathy
CNSLeptomeningeal carcinomatosis instead of parenchymal masses of the brain
OrbitDiffuse expansile infiltration of the postseptal fat causing proptosis instead of enophthalmos as seen in scirrhous invasive ductal carcinoma; fusiform thickening of the extraocular muscles; globe and optic nerve often spared
BoneDiffuse infiltration of the bone marrow, which may cause signal reversal of the bone marrow on unenhanced T1-weighted MRI sequences rather than forming expansile masses

Gastrointestinal Tract

The reported incidence of ILC metastasis in the gastrointestinal system varies greatly. Autopsy series report that 20–43% of ILC tumors metastasize to the gastrointestinal tract [12, 14]. On the other hand, two large tumor registry–based series report incidences of approximately 5% [2, 16]. One possible explanation for such a large discrepancy is that autopsies can reveal clinically occult micrometastases. Nevertheless, the prevalence of gastrointestinal metastases among ILC patients was significantly higher than that among IDC patients in all these series. In one large series in which 57 patients with metastatic ILC were evaluated on CT of the chest, abdomen, and pelvis, Winston et al. [15] found that 18 patients (32%) had gastrointestinal involvement.
When the gastrointestinal tract is involved with metastatic ILC, the stomach and small bowel are the most commonly involved, followed by the colon and rectum. In a series of 27 patients with metastatic breast cancer to the stomach who were seen over 15 years, Taal et al. [22] found that 20 patients (74%) had ILC. In another study of 17 patients with metastatic breast cancer to the colon and rectum over the same period [23], the same authors found that 15 patients (88%) had ILC. A different group of authors, reporting on 35 patients who were seen between 1980 and 2008 and had gastric metastasis from breast cancer, found that 34 patients (97%) had ILC [24]. In a retrospective review of 53 breast cancer patients with gastrointestinal metastasis, McLemore et al. [25] reported that 34 patients (64%) had ILC.
ILC metastases to the gastrointestinal tract mirror the way ILC spreads in the breast. Harris et al. [12] described this pattern as a “diffuse spreading process.” The tumor cells can infiltrate all layers of the bowel wall, causing mural thickening; in contrast, metastatic IDC causes mural masses. Metastatic ILC's diffuse infiltration of the stomach wall can give an appearance of linitis plastica (Fig. 1), which is indistinguishable from primary scirrhous carcinoma of the stomach. Linitis plastica (water-bottle stomach) denotes a diffuse infiltrative neoplastic process that affects the intramural layer of a hollow structure resulting in a shrunken organ with thickened walls. It occurs most commonly in the stomach where it produces circumferential thickening and stiffness of the gastric wall, narrowed lumen, and decreased motility. In one series, all 31 patients with linitis plastica from metastatic breast cancer were found to have ILC [26]. A linitis plastica appearance of the colon from metastatic ILC has also been described [27].
Fig. 1A —65-year-old woman with no known diagnosis of cancer who presented with nausea, vomiting, and diarrhea. Endoscopy was impeded by obstruction at pylorus. Endoscopic biopsy of body and fundus revealed metastatic lobular breast carcinoma. Laparotomy and bowel resection confirmed metastatic infiltrating lobular carcinoma (ILC) to colon, small bowel, and stomach. There were no known hepatic or lung metastases. ILC of left breast was diagnosed at breast imaging workup.
A, Coronal CT scan of abdomen and pelvis obtained with oral contrast material shows diffuse thickening of gastric wall (arrows), which is consistent with linitis plastica.
Fig. 1B —65-year-old woman with no known diagnosis of cancer who presented with nausea, vomiting, and diarrhea. Endoscopy was impeded by obstruction at pylorus. Endoscopic biopsy of body and fundus revealed metastatic lobular breast carcinoma. Laparotomy and bowel resection confirmed metastatic infiltrating lobular carcinoma (ILC) to colon, small bowel, and stomach. There were no known hepatic or lung metastases. ILC of left breast was diagnosed at breast imaging workup.
B, Anteroposterior projection image from upper gastrointestinal series shows fixed nodular narrowing of stomach, especially at antrum and distal body (arrows), giving linitis plastica appearance.

Genitourinary System

Breast cancer in women rarely metastasizes to the genitourinary system. Compared with IDC, ILC has a significantly higher propensity to spread to gynecologic organs [2, 12, 14, 16]. The reported incidence of ILC metastasis to the gynecologic system ranges from 36% to 52% in autopsy series [12, 14] and from 2% to 5% in clinical series [2, 16]. This discrepancy is likely because that autopsy can reveal clinically silent micrometastases. In their series, Winston et al. [15] reported adnexa involvement in 12 patients (21%).
The genitourinary organ that metastatic ILC most commonly involves is the ovary, followed by the uterus. In a series of 29 patients with documented ovarian metastasis at surgery, 12 (41%) had metastatic ILC [28]. ILC metastasis to the ovaries usually presents as bilateral cystic and solid ovarian masses (Krukenberg syndrome) (Fig. 2). Krukenberg tumors are defined as metastasis to one or both ovaries, which contain signet ring cells (mucin producing) that invade the hypercellular ovarian stroma on histopathology. They originate most frequently from the gastrointestinal tract and less commonly from the breast and other organs. Micrometastasis to the ovary may be occult on clinical examination or imaging studies. In a series of 14 patients who had metastatic ILC and were seen at our institution (He H, unpublished data), two patients had occult metastasis to the ovaries at the time of prophylactic hysterectomy and oophorectomy, before initiation of hormonal therapy. CT of the abdomen and pelvis before surgery did not reveal ovarian abnormalities in these patients.
Fig. 2 —25-year-old woman with infiltrating lobular carcinoma (ILC) of breast. Axial contrast-enhanced CT scan of abdomen and pelvis in portal venous phase shows bilateral mixed cystic and solid pelvic masses (arrows) consistent with enlarged ovaries. CT-guided percutaneous core needle biopsy revealed metastatic ILC of breast consistent with Krukenberg syndrome.
In 1993, Le Bouedec et al. [29] reported 12 patients with metastatic breast cancer to the uterus, 10 of whom had ILC. The most common site within the uterine corpus that metastatic ILC involves is the myometrium, followed by the endometrium. The endometrial gland is often spared. Abnormal uterine bleeding may be the first sign of metastasis. Most ILC patients have estrogen receptor–positive tumor and are treated with hormonal therapy, which increases the risk of developing second primary endometrial cancers. Differentiating a primary endometrial malignancy from ILC metastasis can thus be challenging but is crucial because the treatments for these cancers are dramatically different.
Breast cancer metastasis to the uterine cervix is extremely rare, with an estimated frequency of 0.8–1.7% [30]. Only 36 cases have been reported in the literature to date [31, 32]. Given this rarity, the incidence of ILC metastasis to the cervix is unknown. In one autopsy series [12], the authors found that of 14 cases of ILC, six (43%) involved the uterine corpus and only one (7%) involved the cervix. Sporadic cases of ILC metastasis to the vulva have also been reported [3335].
Breast cancer rarely metastasizes to the bladder. Before 2008, only 34 breast cancer patients had been reported to have bladder metastasis [36, 37]. Feldman et al. [38] summarized 19 cases of breast cancer metastasis to the bladder and found that 33% of the cases with identified histologic subtypes were ILC. If this percentage is representative of all bladder metastases from breast cancer, then the rate of ILC metastasis to the bladder is much higher than the 10% prevalence of ILC among breast cancers.
ILC metastasis to the bladder generally results from the extension of disseminated disease from adjacent organs into the bladder; however, isolated bladder metastases, presumably spreading along the retroperitoneal lymphatics, have also been reported [39]. Synchronous breast cancer metastasis to both the bladder and ureter and isolated breast cancer metastasis to the ureter have also been reported [4042].
Complications of breast cancer metastasis to the genitourinary system include ureteral obstruction and hydronephrosis [15, 43] (Fig. 3), retroperitoneal fibrosis [44], and renal failure. In their series, Winston et al. [15] found that six patients (11%) had hydronephrosis.
Fig. 3A —68-year-old woman with history of infiltrating lobular breast carcinoma who presented with abdominal pain, nausea, and vomiting.
A, Axial contrast-enhanced CT scans of abdomen and pelvis show enhancing retrocaval and paraaortic retroperitoneal adenopathy (arrows, A), left ureteral implant and mild hydroureter (arrow, B), and bilateral hydronephrosis (arrows, C).
Fig. 3B —68-year-old woman with history of infiltrating lobular breast carcinoma who presented with abdominal pain, nausea, and vomiting.
B, Axial contrast-enhanced CT scans of abdomen and pelvis show enhancing retrocaval and paraaortic retroperitoneal adenopathy (arrows, A), left ureteral implant and mild hydroureter (arrow, B), and bilateral hydronephrosis (arrows, C).
Fig. 3C —68-year-old woman with history of infiltrating lobular breast carcinoma who presented with abdominal pain, nausea, and vomiting.
C, Axial contrast-enhanced CT scans of abdomen and pelvis show enhancing retrocaval and paraaortic retroperitoneal adenopathy (arrows, A), left ureteral implant and mild hydroureter (arrow, B), and bilateral hydronephrosis (arrows, C).

Peritoneum and Retroperitoneum

Compared with IDC, ILC has a much higher propensity to metastasize to the peritoneum and retroperitoneum. Autopsy series reported the metastasis rates of ILC to the peritoneum and retroperitoneum ranging from 60% to 93% [12, 14], and a clinical series reported a rate of 3% [2]. Winston et al. [15] reported peritoneal involvement in 17 patients (30%) and retroperitoneal involvement in nine patients (16%).
The pattern of ILC spread in the peritoneum and retroperitoneum is distinct in that the metastases form tiny nodules that tend to become confluent and may cause “omental caking” [12]. In contrast, IDC spread in the peritoneum and retroperitoneum often presents as larger masses and nodules.
Peritoneal carcinomatosis with ascites (Fig. 4) may accompany the metastasis of ILC to the gastrointestinal tract and carries a grave prognosis [45]. The retroperitoneal spread of ILC may cause retroperitoneal adenopathy (Fig. 3), ureteral obstruction, hydronephrosis, and retroperitoneal fibrosis [44].
Fig. 4A —25-year-old woman with infiltrating lobular carcinoma (ILC) of breast (same patient as in Fig. 2).
A, Axial contrast-enhanced CT scan of abdomen and pelvis in portal venous phase shows numerous tiny nodular soft-tissue deposits (thick arrow) in peritoneal fat of left lower quadrant of abdomen consistent with carcinomatosis. Patient had right ureteral stent (thin arrow) for obstructive hydronephrosis (not shown), likely caused by large ovarian masses shown in Figure 2. Soft tissue surrounding right ureteral stent may be inflammation or metastatic deposits from ILC.
Fig. 4B —25-year-old woman with infiltrating lobular carcinoma (ILC) of breast (same patient as in Fig. 2).
B, Axial contrast-enhanced CT scan of abdomen and pelvis in portal venous phase shows ascites (arrows) in upper abdomen.

Bone and Bone Marrow

In their series, Winston et al. [15] reported that the most common site of ILC metastasis was bone. In that study, 46 patients (81%) developed bone metastases. In a series of 14 patients who had metastatic ILC and were seen at our institution (He H, unpublished data), nine patients (64%) had bone metastasis. Some studies have found that the rate of bone metastasis of ILC patients is higher than that of IDC patients [2, 13, 46], but other studies did not find such a difference [12, 16, 18].
Similar to its diffuse spread in the breast and other organ systems, ILC infiltration into the bone marrow results in the total replacement of the bone marrow rather than the formation of expansile masses. The total replacement of bone marrow by metastatic ILC may cause signal reversal of bone marrow on T1-weighted MRI (Fig. 5). On 18FFDG PET/CT images, diffuse bone metastases appear as numerous “hot spots,” or areas of increased FDG uptake, throughout the skeleton (Fig. 6).
Fig. 5 —25-year-old woman with infiltrating lobular breast carcinoma (same patient as in Fig. 2). Sagittal unenhanced T1-weighted MR image of lumbar spine reveals diffuse decreased signal intensity of bone marrow consistent with neoplastic infiltration of thoracolumbar spine. Normal bone marrow has higher signal than intervertebral disks.
Fig. 6 —53-year-old woman with metastatic infiltrating lobular breast carcinoma. Maximum-intensity-projection whole-body PET/CT scan reveals numerous foci of increased FDG uptake throughout skeleton, consistent with widespread bone metastasis.

CNS and Orbit

In contrast to IDC metastasis to the CNS, which tends to form metastatic masses in the brain parenchyma, ILC that metastasizes to the CNS has a strikingly high propensity to spread diffusely along the leptomeninges. In one series [12], for example, nine of 10 ILC patients with CNS involvement had carcinomatous meningitis, whereas only one of 16 IDC patients with CNS involvement had carcinomatous meningitis. In another series, Smith et al. [47] found that of 365 patients with advanced breast carcinoma, 19 (5.2%) had cerebral parenchymal deposits that were almost exclusively associated with IDC. They also found that 10 patients (2.7%) developed meningeal infiltration that was almost exclusively associated with ILC. On contrast-enhanced MRI, ILC involving the leptomeninges presents as enhancement of the leptomeningeal linings (Fig. 7).
Fig. 7 —25-year-old woman with infiltrating lobular breast carcinoma (same patient as in Fig. 2). Sagittal contrast-enhanced fat-saturated T1-weighted MR image of lumbar spine reveals abnormal leptomeningeal enhancement of lumbar thecal sac (thin arrow) and nodularity of cauda equina (thick arrow). Analysis of CSF via lumbar puncture revealed carcinomatosis.
The incidence of ILC metastasis to the orbit is unknown, although a few cases have been reported [4850]. In our series of 14 patients with metastatic ILC, three patients (21%) had orbital metastasis. In this small series, metastatic ILC involved the extraocular muscles with diffuse fusiform thickening and enhancement of the muscles on contrast-enhanced MRI. Diffuse infiltrative enhancing soft tissue replacing the postseptal fat or connective tissue often accompanies the abnormally enhancing extraocular muscles (Fig. 8). This diffuse infiltrative expansile process often causes proptosis. The Tenon capsule, sclera, and eyelid soft tissue may also be involved [48, 51]. The optic nerve and globe are spared. In contrast, metastasis of scirrhous IDC to the eye may cause enophthalmos, blepharoptosis, and ocular palsy, presumably secondary to a mechanism similar to scar contracture.
Fig. 8 —25-year-old woman with infiltrating lobular breast carcinoma who presented with left proptosis (same patient as in Fig. 2). Axial contrast-enhanced fat-saturated T1-weighted MR image of orbit reveals fusiform thickening and abnormal enhancement of left lateral rectus muscle (thin white arrow) and diffuse infiltrative postseptal soft tissue replacing fat (thick white arrow). Optic nerve (black arrow) and globe (star) are spared.

Other Sites

The rates of ILC and IDC metastasis to the liver do not differ significantly [2, 12, 14, 16]. Similar to IDC, ILC that metastasizes to the liver presents as multiple enhancing masses within the hepatic parenchyma (Fig. 9) and is indistinguishable from other metastatic disease. ILC rarely metastasizes to the gallbladder [5254] with infiltration of the gallbladder wall (muscularis layer and adventitia) (Fig. 10). Patients may be asymptomatic or may present with acute cholecystitis.
Fig. 9 —64-year-old woman with metastatic infiltrating lobular breast carcinoma. Axial contrast-enhanced CT scan of abdomen and pelvis in portal venous phase reveals multiple enhancing masses within hepatic parenchyma consistent with bilobed metastases.
Fig. 10 —54-year-old woman who presented with early satiety and right upper quadrant pain. Axial contrast-enhanced CT scan of abdomen and pelvis in portal venous phase reveals mild thickening of gallbladder wall (arrow). Resection of gallbladder revealed metastatic infiltrating lobular breast carcinoma.
ILC spreads to the lungs and pleura less frequently than IDC does [2, 12, 14, 16]. The imaging characteristics of metastatic ILC including pulmonary nodules and malignant pleural effusion are similar to those of IDC (Fig. 11).
Fig. 11A —64-year-old woman with history of infiltrating lobular breast carcinoma (same patient as in Fig. 9).
A, Axial contrast-enhanced CT scan of chest shown using lung window settings reveals multiple new pulmonary nodules (arrows) consistent with metastasis.
Fig. 11B —64-year-old woman with history of infiltrating lobular breast carcinoma (same patient as in Fig. 9).
B, Axial contrast-enhanced CT scan of chest shown using soft-tissue window settings reveals new bilateral pleural effusions (arrows); cytologic analysis showed lobular carcinoma.
Several case reports have described ILC metastasis to soft tissues [55, 56]. ILC that metastasizes to subcutaneous locations often presents as painless nodules (Fig. 12).
Fig. 12A —61-year-old woman with metastatic infiltrating lobular breast carcinoma.
A, Axial contrast-enhanced CT scan of chest reveals large left breast mass (short arrow), large malignant left pleural effusion (stars), and total collapse of left lung (long arrow).
Fig. 12B —61-year-old woman with metastatic infiltrating lobular breast carcinoma.
B, Axial contrast-enhanced CT scan of abdomen and pelvis in portal venous phase reveals multiple enhancing subcutaneous nodules (arrows) consistent with metastasis. Star denotes large left breast mass that had grown into abdominal wall.

Conclusion

In summary, this review of the pattern of ILC metastasis emphasizes its presentation at unusual sites such as the gastrointestinal tract, genitourinary system, peritoneum, retroperitoneum, bone, bone marrow, CNS, leptomeninges, and orbit. This knowledge may aid in accurate imaging interpretation and treatment planning in patients with metastatic ILC of the breast.

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 1140 - 1148
PubMed: 24758672

History

Submitted: April 23, 2013
Accepted: July 30, 2013

Keywords

  1. infiltrating lobular carcinoma of the breast
  2. invasive lobular carcinoma of the breast
  3. metastatic disease

Authors

Affiliations

Hongying He
Department of Diagnostic and Interventional Imaging, The University of Texas Health Science Center at Houston, 6431 Fannin St, MSB 2.130B, Houston, TX 77030.
Anneliese Gonzalez
Division of Oncology, Department of Internal Medicine, The University of Texas Health Science Center at Houston, Houston, TX.
Emily Robinson
Department of Surgery, The University of Texas Health Science Center at Houston, Houston, TX.
Wei T. Yang
Department of Diagnostic Radiology, Division of Diagnostic Imaging, Breast Imaging Section, The University of Texas M. D. Anderson Cancer Center, Houston, TX.

Notes

Address correspondence to H. He ([email protected]).

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