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 Table of Contents  
Year : 2017  |  Volume : 3  |  Issue : 3  |  Page : 101-105

Gastric metastases mimicking primary gastric cancer: A brief literature review

1 Department of Pathology, University of Medicine and Pharmacy, Târgu Mureş; Department of Pathology, Clinical County Emergency Hospital, Târgu Mureş; Department of Pathology, Research Center of University of Medicine, Târgu Mureş, Romania
2 Department of Pathology, University of Medicine and Pharmacy, Târgu Mureş, Romania
3 Department of Pathology, Clinical County Emergency Hospital, Târgu Mureş, Romania

Date of Submission30-Nov-2016
Date of Acceptance23-Feb-2017
Date of Web Publication8-Jun-2017

Correspondence Address:
Simona Gurzu
Department of Pathology, University of Medicine and Pharmacy, 38 Ghe Marinescu Street, 540139 Târgu Mureş
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ctm.ctm_67_16

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Gastric cancer is the fifth most common cancer worldwide, with most cases presenting in the form of primary tumors. In this paper, we performed a literature review on the incidence and particularities of extragastric metastases. These lesions are rare in clinical practice and can be misdiagnosed as primary undifferentiated gastric carcinomas as the differential diagnosis between primary and secondary malignancy is difficult to make. As per the literature, the most common malignancies which can present gastric metastases are lung cancer, followed by carcinoma of the breast, esophagus, kidney, and head and neck carcinomas. Malignant melanoma, ovarian cancer, prostate cancer, and adrenal gland carcinomas are rarely described as presenting metastases in the stomach. In most cases, the literature addressed poorly differentiated tumors with high-grade malignancy. The most common feature was the ulcerated tumor with depressed area, associated with identifiable extragastric tumor cells in the gastric submucosa. The linitis plastica-like feature is unusual and is more characteristic of breast lobular carcinoma. The accurate diagnosis of such rare extragastric metastatic cases depends on the appropriate clinical history and precise pathological diagnosis, which is mandatory for initiating the best therapeutic options.

Keywords: Breast, gastric cancer, gastric metastasis, stomach

How to cite this article:
Gurzu S, Beleaua MA, Banias L, Jung I. Gastric metastases mimicking primary gastric cancer: A brief literature review. Cancer Transl Med 2017;3:101-5

How to cite this URL:
Gurzu S, Beleaua MA, Banias L, Jung I. Gastric metastases mimicking primary gastric cancer: A brief literature review. Cancer Transl Med [serial online] 2017 [cited 2019 Aug 18];3:101-5. Available from: http://www.cancertm.com/text.asp?2017/3/3/101/203893

  Introduction Top

Although screening programs have been introduced in most countries, gastric cancer (GC) still remains one of the tumors which are diagnosed in advanced stages and also represents the second leading cause of cancer-associated death worldwide.[1] Although the latest therapeutic guidelines indicate preoperative chemotherapy, followed by surgery, in some medical centers, gastrectomy is still performed as the first therapy of choice. Since most cases are primary tumors, the suspicion of metastatic involvement of the stomach is rarely taken into consideration. It is difficult to differentiate between a primary and a metastatic tumor in the stomach, especially in cases that show mucosal infiltration.[2],[3],[4],[5]

The present paper is a review of the literature on the incidence and particularities of gastric metastases of extragastric malignancies. The online search was performed using the PubMed database. Keywords such as “gastric metastasis,” “gastric metastasis from,” “metastatic gastric carcinoma from,” and “gastrointestinal metastases” were used to identify studies referring to gastric metastasis, published between 1980 and 2016. Only publications in English and referring to human tissues were considered [Figure 1].
Figure 1: The methodology used for the study

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Gastric Metastases – General Aspects

The autopsy examinations revealed that the incidence of gastric metastasis accounts for about 0.2%–1.7% of all metastatic cases.[6],[7],[8] The clinical symptoms of patients with blood-borne or lymphatic-borne gastric metastases are similar to those occurring in patients with primary GC. Gastric metastases are seen in patients with a median age of 56–58 years (range, 28–82 years), with symptoms of hematemesis, melena, weight loss, nausea, vomiting, dyspepsia, epigastric pain, refractory anemia, etc.[6],[7],[8] In GC patients, the suspicion of gastric metastasis can be based on the medical history of a previous extragastric malignant tumor. However, mostly, the diagnosis can only be established microscopically.

An endoscopic examination can reveal an ulcerated tumor, but the most common aspect of the metastatic tumor is its “bull's eye sign” or “volcano-like ulcer.”[3],[6],[7] This refers to a depressed area covered by intact mucosa or an elevated submucosal tumor that is ulcerated at the apex, which can also imitate a lymphoma, a gastrointestinal stromal tumor, or a schwannoma.[3],[6],[9] The “bull's eye sign” occurs in 44%–77% of cases.[2],[3],[6] In 51%–62% of cases, solitary gastric lesions are identified; however, multiple metastatic tumors can also occur, predominantly located in the middle or upper third of the stomach.[6],[7],[10] A linitis plastica-like aspect is rare and lesions such as polyps, flat ulcers, and elevated plaques are unusual in metastasized GC tumors.[4],[5],[6],[11] As the mucosa can be intact, it is not always identified during regular endoscopy.[5],[7] Since classic endoscopic biopsies are inadequate for a definite diagnosis, the endoscopic ultrasound-fine needle aspiration biopsy is currently the standard accepted method for the diagnosis of submucosal tumors. Using this technique, the diagnosis is feasible in more than 40% of cases.[9]

Gastric metastasis usually occurs in a metachronous manner. The median interval between the diagnosis of a nongastric primary tumor and gastric metastasis is roughly 13 months (range, 1–34 months).[10] Due to the difficulty of microscopically examining the biopsy specimens, the presumptive diagnosis is usually the “undifferentiated carcinoma.”[7],[12],[13],[14] The absence of gastric epithelial dysplasia was suggested for consideration of extragastric metastasis, but this does not exclude a primary GC.[12] The correct diagnosis is based on medical history and the tumor immunoprofile, which is not always persuasive. The examination of tumor specimen, obtained from gastrectomy, generally shows an intact mucosa with tumor cell clusters or cords in the submucosa as well as into the underlying layers of the stomach. The foveolar layer is generally intact and the tumor cells are located in the deep glandular layer.[4],[5] In case of a mucosal infiltration, the difficulty of differential diagnosis is increased.[6],[7]

  Gastric Metastases from Breast Cancer Top

It was reported that in 13.5%–33% of extragastric metastases, the primary tumors were located in the breast.[2],[7],[10] Gastric metastases generally occur at a median interval of 36–84 months after diagnosis of the primary tumor.[2],[7],[15],[16] Metastasis to gastrointestinal tract was reported even as late as 20–30 years from an initial diagnosis of breast cancer.[17] They are mostly located in the gastric fundus (43%) and pylorus (43%).[15],[16] A report shows that the gastrointestinal metastasis occurs only in 32% of breast cancer cases and carcinomatosis is associated in 25% of the patients.[18] In other case series, it was observed that other organs were concomitantly affected in 94% of breast carcinoma patients with gastric metastasis.[19]

Considering the histological type, the lobular infiltrating breast carcinomas are more predisposed to producing gastric metastases, compared to ductal types.[4],[5],[20] Roughly 85%–97% of breast carcinoma-derived gastric metastases are from lobular variant.[15],[21] It was reported that 3%–18% of the lobular infiltrating breast carcinomas can present gastric metastases even several years after diagnosis.[4],[22] Due to the high vascularity of the breast cancer, metastases can occur in any organ and tissues including skin, pleura, peritoneum, and ovaries,[4],[5] with the possibility of stomach being the first place of presentation in some cases.[22]

The gastric metastasis from lobular breast cancer can be a protruded lesion or present a linitis plastica-like feature.[4],[5],[6] The lobular breast cancer-induced syndrome of linitis plastica was first reported in 1980 by Cormier et al.[23] Under endoscopy, the metastatic ductal-type breast carcinoma is usually a solitary tumor that shows the “bull's eye sign.”[4] External compression of the cardia, pylorus, or duodenum can occur due to metastatic breast cancer.[21],[24],[25],[26]

The immunoprofiling of tumor cells can elucidate the diagnosis but is not always helpful. In some cases, a large panel of antibodies is used for the final diagnosis. Breast cancer cells show positive reaction to estrogen receptors (ERs) (in 72%–90% of the cases), mammaglobin (48%–80%) and rarely to progesterone receptors (PRs) (33%).[4],[5],[22],[27] However, the positivity for these hormonal receptors can be lost in the metastatic tissue, following hormonal therapy.[4],[5],[28] To complicate further, both ER and PR inconsistently mark the primary gastric carcinoma cells in up to12% of the cases.[4],[5],[22],[27]

E-cadherin negativity is rarely observed in primary GCs and can be of use to diagnose lobular metastatic carcinoma. However, the difficulty of diagnosis increases in patients with synchronous or metachronous hereditary diffuse gastric carcinoma (HDGC), and thus, in young patients with E-cadherin negative GCs, a primary HDGC should also be taken into account.[1],[29]

Cytoplasmic positivity for gross cystic disease fluid protein (GCDFP15) and/or GATA3 can prove the breast origin of tumor cells.[4],[22] GCDFP15-positive cells are identified in 78% of breast cancer, with no positivity for the primary GC.[27],[30] In contrast, MUC6 and CDX2 are expressed in 39% and 67% of GCs, respectively, with no positivity for breast cancer.[27] Further, the primary GC cells are positive for carcinoembryonic antigen while the breast cancer cells are negative.[30]

Cytokeratins (CKs) have a limited value in differential diagnosis of GC.[5],[22],[27] Although the CK7+/CK20 immunoprofile is characteristic of tumor cells of breast origin, about 33% of the primary GC cells exhibit same profile.[5],[22] The CK5/6 is expressed in 61% of breast carcinoma cells and 16% of primary GC cells.[27] The CK20+/ER pattern is an indicator of the primary tumor of the stomach.[31]

Following diagnosis of gastric metastasis, the median survival period of the patients is 10–28 months (ranging from 1 to 84 months) and even lower in patients with multiorganic metastases.[16],[18],[22],[24] The 2-year survival rate is 22%–53%.

Only 9% of all breast carcinomas with gastric metastasis show HER-2 positivity [15] and can be effectively treated with trastuzumab. The Ki67 index and HER-2 expression are usually identical in the primary and metastatic gastric tumor cells.[28],[32]

Cases with linitis plastica-like metastasis from a lobular breast cancer that displays positivity for the hormonal receptors show good response to hormone therapy, along with tamoxifen or classic chemotherapy.[18],[21],[30],[33] The benefits of gastrectomy in these patients are still under debate.[19]

In a rare case that was recently published, the occurrence of gastric metastasis as the first symptom of a lobular breast carcinoma with a long period of latency before presentation of the primary breast carcinoma was reported.[34] First, the case was diagnosed on a gastric biopsy specimen as a primary T2N0M0 signet ring cell gastric carcinoma, and the patient was treated with chemoradiotherapy using two cycles of 5-fluorouracil and cisplatin. Then, total gastrectomy was performed and the specimen revealed dissociated cells in all of the gastric wall layers, including the mucosa. The patient received an additional six cycles of tegafur and calcium folinate postoperatively. The breast tumor that was seen at 14 months following the diagnosis of GC was staged at mammography as a T3N0 metachronous breast cancer. The diagnosis of invasive breast lobular carcinoma was established after examination of the core biopsy specimen that was positive for ER and PR without E-cadherin expression. After six cycles of chemotherapy (docetaxel, epirubicin, and cyclophosphamide) and hormonotherapy for breast cancer without mastectomy, the patient was in remission after 23 months. Further, multiple inoperable metastatic tumors occurred in the colon and rectum, after which all of the specimens (gastric resections and biopsies from the breast, colon, and rectum) were reexamined providing the final diagnosis as “breast invasive lobular carcinoma with a signet ring cell aspect, with gastric and colorectal metastases.” The metastatic tumor cells displayed the same immunoprofile as the breast cancer cells. The patient died 86 months after the diagnosis of gastric metastasis.[34] This case highlights the difficulty of diagnosing gastric metastases.

  Gastric Metastases from Lung Cancer Top

It was reported that in 19%–55% of gastric metastases, the primary tumors were located in the lungs.[2],[6],[7],[10] It was proven by autopsy-based studies that about 0.2%–0.7% of all lung tumors present gastric metastases.[6] Considering the histological types, adenocarcinomas were found more predisposed to showing gastric metastases (27%), followed by small cell carcinomas (16%), squamous cell carcinomas (10%), and epithelioid tumors.[6],[10],[13]

For the pulmonary adenocarcinoma patients with gastric metastases and activated epidermal growth factor receptor (EGFR) mutations, gastrectomy followed by chemotherapy with anti-EGFR erlotinib can increase the overall survival rate to about 4 years following the diagnosis.[13] A proper diagnosis is mandatory for a satisfactory therapy. A differential diagnosis is difficult to conclude and is based on the clinicopathological information correlated with the tumor cells' positivity for thyroid transcriptional factor-1 (TTF1), which is an indicator for pulmonary origin. Both pulmonary adenocarcinoma and GC cells were positive for CK 7, while CDX2 positivity indicates gastrointestinal origin.[13]

  Gastric Metastases from Other Carcinomas Top

In addition to breast and lung cancers, gastric metastases were also reported as arising from carcinomas originating in the following organs: esophagus (8%–19% of cases), kidneys (3%–8%), head and neck (1%–6.2%), uterus (6%), colorectum (5%), ovary (8%–10%), bladder (3%), brain (3%), prostate, testes (seminoma), adrenal glands, liver, pancreas, skin, and others.[2],[10],[35],[36]

Among the head and neck cancers, salivary duct carcinomas, especially those originating from the parotid gland, were reported to present gastric metastases in 0.8%–5.4% of cases.[35] Most of these were squamous cell carcinomas.[6] Thyroid carcinomas have a low metastatic potential, with gastric metastases being described in only one case of medullary carcinoma, 25 years after the resection of the primary tumor.[36] In anaplastic thyroid carcinomas, hematogenous spread is more frequent and about 4% of metastatic cases present gastric involvement.[37],[38]

Gastric metastasis of hepatocellular carcinoma (HCC) is a rare condition that occurs through hematogenous spread.[39] The HCC metastases can occur at multiple sites across the gastrointestinal tract, including stomach, even 5 years after diagnosis of the primary tumor.[40] Moreover, the primary GC can show hepatoid metaplasia with focal positivity for alpha-fetoprotein, which increases the difficulty of diagnosis.[6]

Prostate adenocarcinomas present a low risk for gastric metastases, with the reported incidence being 1%–4% of all prostate carcinomas.[8] Carcinomas with acinar differentiation have a higher risk for lymphatic or hematogenous route-based gastric metastases, compared to ductal adenocarcinomas.[8],[14] In inoperable cases with gastric metastases, the survival rate is as low as 4 months.[8] Late metastases were described at 33–46 months following prostatectomy,[8],[13] with survival time after developing gastric metastases being 3–23 months.[8] Diagnosis is based on the positivity of the prostate tumor cells for alpha-methylacyl-coenzyme A racemase (AMACR, P504S) and prostate-specific antigen (PSA).[8],[13],[41] The differential diagnosis should consider primary GCs such as epithelioid gastrointestinal stromal tumor (marked by C-KIT and DOG-1) and oncocytic variant of a neuroendocrine tumor (displays positivity for neuroendocrine markers such as chromogranin and synaptophysin).[12] The PSA serum level is generally elevated and the majority of cases do not respond at hormonal therapy.[8],[41],[42] Clinical symptoms that may raise the suspicion of gastrointestinal tract metastasis are persistent iron deficiency anemia, nausea, and vomiting.[12],[41],[42]

Merkel cell carcinoma (MCC) is a rare, aggressive cutaneous tumor with neuroendocrine differentiation and a high risk for systemic metastases.[43],[44],[45] Gastric metastases from MCC were reported in very few cases as a single lesion or multiple gastrointestinal metastases occurring at about 4 months after the diagnosis of MCC.[43],[46] Without the clinical history, MCC metastases can easily be confused with primary undifferentiated gastric carcinoma as both display positivity for CK20.[43] A useful approach in this instance is to realize that primary GCs display diffuse cytoplasmic positivity for CK20, while a perinuclear dot-like staining pattern is the characteristic of MCC.[44],[45],[46] MCC cells are marked by neuroendocrine markers such as chromogranin, which are also expressed by the primary neuroendocrine tumors of the stomach.[43]

The differential diagnosis for metastatic MCC should include small B-cell lymphoma (which is positive for leukocyte common antigen but does not mark MCC cells) and gastric metastases from other malignancies, such as anaplastic small cell melanomas (which are marked by the specific markers HMB45 and S-100) and small cell carcinoma of lung (which is positive for TTF-1 and can present neuroendocrine features and even CK20 positivity).[44],[46] MCC can also infrequently show TTF-1 positivity.[44]

Metastasis from choriocarcinomas is unusual and can be confused with primary gastric choriocarcinomas, which can display focal positivity for human choriogonadotropin. In patients with testicular or extragonadal choriocarcinomas, upper gastrointestinal bleeding can be the first clinical sign. The metastatic cells are seen in the gastric submucosa but can also infiltrate other gastric wall layers.[47],[48]

Only one case of nonfunctional sporadic adrenocortical carcinoma with gastric metastasis was reported in 2016 in a 71-year-old male hospitalized for GC. The endoscopic specimen diagnosis was “undifferentiated carcinoma.” Following gastrectomy, in the surgical specimen, the metastatic tumor cells were identified within the gastric submucosa. Then, the final diagnosis of “nonfunctional sporadic adrenocortical carcinoma with gastric metastasis” was established based on the nonmodified mucosa, the architecture of the tumor cells (large polygonal cells with slight basophilic, eosinophilic, or vacuolated cytoplasm, pleomorphic nuclei, and a high mitotic rate), and their immunoprofile (positivity for vimentin, inhibin, synaptophysin, neuron-specific enolase, and calretinin).[49]

  Gastric Metastases from Melanomas Top

Gastrointestinal metastases of melanoma are generally identified in the small bowel (81%) and colon (15%), with the stomach being involved in only 4% of metastatic cases.[50] However, 7%–27% of gastric metastases originate from cutaneous melanoma and 26% of all melanomas can present gastric involvement.[2],[3],[6],[7]

Macroscopically, the melanoma metastases are generally identified as umbilicated submucosal nodules, but an infiltrative aspect was also described.[3],[50] The final diagnosis is based on the patient's history of melanoma, the infrequent presence of melanin pigment, and the tumor cells' architecture and immunoprofile. The specific markers of melanoma cells include S-100 protein, HMB45, melan A, and SOX-10.[3] The survival rate of patients with gastric metastatic melanoma ranges between 3 and 13 months.[3]

  Conclusion and Future Perspectives Top

The data published in the literature concerning metastatic tumors of the stomach are incomplete, and most papers were published as case reports. The real incidence of stomach metastases remains unknown. Individualized therapy has significantly increased the overall survival rates, and thus, the number of cases with gastric metastases occurring several years after therapy will likely increase. Large studies are necessary to elucidate the particular features of these tumors. In addition, histological diagnosis of any gastric undifferentiated carcinomas should consider the possibility of a metastatic tumor, which is crucial for future oncological therapy.

Financial support and sponsorship

This work was partially supported by the University of Medicine and Pharmacy of Tirgu-Mures, Romania, team research projects frame: UMFTGM-PO-CC-02-F01 – No. 19/2014.

Conflicts of interest

There are no conflicts of interest.

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