Layered enhancement with punctate foci of calcifications: A unique computed tomographic feature of mucinous adenocarcinoma of stomach

Sourav Bera; Jyotibash Sahoo; Mahamaya Sharma; Pradosh Kumar Sarangi; Prasanta Kumar Majumdar

doi:10.4103/oji.oji_2_23

CASE REPORT

Year : 2023 | Volume : 7 | Issue : 1 | Page : 17-20

Layered enhancement with punctate foci of calcifications: A unique computed tomographic feature of mucinous adenocarcinoma of stomach

Sourav Bera¹, Jyotibash Sahoo¹, Mahamaya Sharma², Pradosh Kumar Sarangi³, Prasanta Kumar Majumdar¹
¹ Department of Radiology, Central Hospital, South-Eastern Railway, Kolkata, West Bengal, India
² Department of Pathology, Central Hospital, South-Eastern Railway, Kolkata, West Bengal, India
³ Department of Radiology, All India Institute of Medical Sciences, Deoghar, Jharkhand, India

Date of Submission	27-Mar-2023
Date of Decision	04-Apr-2023
Date of Acceptance	05-Apr-2023
Date of Web Publication	26-Apr-2023

Correspondence Address:
Pradosh Kumar Sarangi
Department of Radiology, All India Institute of Medical Sciences, Deoghar, Jharkhand
India

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/oji.oji_2_23

Abstract

Calcifications are rare in gastric adenocarcinoma and all reported cases correspond to a mucinous adenocarcinoma. Mucinous gastric adenocarcinoma (MGC) is a rare histological variety representing approximately 2.6%–6.6% of gastric cancers, sometimes associated with punctate and miliary calcification. We describe one such case having punctate calcifications with characteristic contrast-enhanced computed tomography showing hypoenhancing middle and outer layer of stomach suggestive of extracellular mucin pool, primarily in submucosa and deeper layer and thin enhancing inner layer suggestive of normal mucosa, referred to as layered enhancement pattern. We also describe the radiopathological correlation of MGC with brief review of literature.

Keywords: Computed tomography, layered enhancement, mucin, mucinous gastric adenocarcinoma, punctate calcification

How to cite this article:
Bera S, Sahoo J, Sharma M, Sarangi PK, Majumdar PK. Layered enhancement with punctate foci of calcifications: A unique computed tomographic feature of mucinous adenocarcinoma of stomach. Oncol J India 2023;7:17-20

How to cite this URL:
Bera S, Sahoo J, Sharma M, Sarangi PK, Majumdar PK. Layered enhancement with punctate foci of calcifications: A unique computed tomographic feature of mucinous adenocarcinoma of stomach. Oncol J India [serial online] 2023 [cited 2023 Jun 4];7:17-20. Available from: https://www.ojionline.org/text.asp?2023/7/1/17/374814

Introduction

Gastric adenocarcinoma is classified into various subgroups, most common being the tubular adenocarcinoma, followed by papillary variant.^[1] Gastric mucinous adenocarcinoma (MGC) is a rare histological variant, accounting for ~2.6%–6.6% of all gastric carcinoma cases with unfavorable outcome compared to nonmucinous gastric carcinomas (NMGC).^[2],[3] Fortunately, the imaging characteristics on contrast-enhanced computed tomography (CECT) described as layered enhancement which is thin enhancing inner layer and hypoenhancing middle and outer layer of the stomach in addition to punctate calcific foci give a diagnostic clue and may help in confident diagnosis.

Case Report

A 52-year-old male patient presented with epigastric pain, intermittent vomiting, melena, and loss of appetite for about the past 3 months. There was no significant medical or surgical history. On clinical examination, a diffuse lump was palpable at the epigastric region. The patient was sent for ultrasound evaluation which showed diffuse heteroechoic thickening of the stomach wall involving distal body and pylorus, with maximum thickness measuring 2.5 cm [Figure 1]. Few foci of calcification were also seen within the thickened stomach wall. There was no obvious increased vascularity in the gastric wall. There was no evidence of retroperitoneal lymphadenopathy. Mild ascites was seen at perihepatic, perigastric area and in pelvis. Rest of the abdomen was unremarkable.

Figure 1: Ultrasonography of upper abdomen showing diffuse heteroechoic thickening of stomach wall (white arrow) involving distal body and pylorus with few foci of calcification (yellow arrow)

Click here to view

For further characterization of the lesion, multiphasic CECT scan of abdomen was done, which showed diffuse circumferential symmetrical gastric wall thickening (maximum thickness – 29.6 mm), involving distal body, antrum, and pylorus [Figure 2]. Multiple punctate calcifications were seen, primarily in middle and outer layer of stomach wall. Layered enhancement pattern was seen in arterial and portal venous phase where significant enhancement (hounsfield unit [HU] = 54) was seen in innermost layer (mucosa) but no perceptible enhancement (HU = 19–24) demonstrated in middle and outer layer of thickened stomach wall. Moderate volume of fluid collection (HU: 18–20) was seen in perigastric, perihepatic, and perisplenic region with multiple areas of liver surface scalloping, suggestive of mucinous ascites with pseudomyxoma peritonei [Figure 3]. Diffuse omental fat standing and nodularity were seen, suggestive of omental caking. A few enhancing lymph nodes were noted in perigastric region, largest measuring 9 mm near greater curvature of the stomach. Moderate-free fluid was present in the pelvis. There was mild splenomegaly (craniocaudal length – 13.6 cm). The liver was normal in size and enhancement pattern without any focal lesions.

Figure 2: (a and b) Noncontrast and postcontrast axial computed tomography image at the same level demonstrates enhancement of innermost layer (Hounsfield unit = 54) (orange arrow), hypoenhancement of middle and outer layer of thickened stomach wall (selected region of interest defined by circle). Noncontrast axial image, (c) showing foci of calcifications (thin white arrow). Postcontrast axial image, (d) at lower abdomen showing ascites and omental caking (white thick arrow)

Click here to view

Figure 3: (a and c) Postcontrast coronal image and (b and d) postcontrast axial images demonstrate scalloping of liver surface (white arrow) at multiple places, surrounded by mucinous ascites. An enhancing perigastric lymph node (elbow arrow) is seen in image d

Click here to view

The patient was given diagnosis of carcinoma stomach, probably mucinous variety along with pseudomyxoma peritonei from imaging findings alone. Differential diagnosis thought was gastric lymphoma and scirrhous adenocarcinoma/signet cell adenocarcinoma, gastric metastasis.

Subsequently, the patient underwent upper gastrointestinal (GI) endoscopy with endosonography. Diffuse abnormal stomach wall thickening was found involving distal body, antrum, and pylorus with submucosal extension. Diffuse erythematous gastric mucosa was seen. Endosonography-guided tru-cut punch biopsy taken for histopathology and it was confirmed to be a mucinous adenocarcinoma of stomach [Figure 4].

Figure 4: Photomicrograph of mucinous carcinoma of the stomach (biopsy), showing (a) prominent glandular formation (blue arrow) floating in extracellular mucin (H and E, ×400), (b) plenty of muciphages (white arrow) in extracellular mucin (H and E, ×400), extracellular abundant mucin deposition (white arrow head) (H and E, ×40) (c and d)

Click here to view

At present, the patient is under chemotherapy with docetaxel, oxaliplatin, leucovorin, and 5-fluorouracil regimen. He has received five cycles of chemotherapy till date, but there has been no significant clinical improvement.

Discussion

Gastric cancer is the fourth most commonly diagnosed cancer and the second most common cause of cancer-related death worldwide.^[1] The prognosis of advanced-stage cancer is still very poor in the present day.

Marked heterogeneity persists in histological classification both at architectural and cytological levels. Recently published the WHO classification (5^th edition, 2019) broadly classifies the stomach tumor into benign epithelial tumors, precursors, and malignant epithelial tumors. Adenocarcinoma is the most common malignant type (95%), which is divided histologically into 12 variants. Among them, tubular, papillary, mucinous, and signet-ring are four major histologic subtypes.^[1]

Mucinous gastric carcinoma (MGC) is defined as a gastric adenocarcinoma with a substantial amount of extracellular mucin (over 50% of tumor volume) within the tumors.^[4] Mucinous carcinoma in the GI tract has worse prognosis than NMGC because they are more frequently diagnosed in the advanced stage and are associated with deeper cancer depth, higher incidence of lymph node metastasis, lymphatic and venous permeation, and peritoneal dissemination.^[5]

Upper GI endoscopy is the most sensitive as well as specific for the detection of gastric cancer. It allows direct visualization of the mucosal irregularity or growth, taking sample for tissue diagnosis and also to assess Helicobacter pylori infection.^[6] However, according to one study, the diagnostic sensitivity of MGC by endoscopic biopsy is relatively low due to the presence of tumor cells predominantly in the submucosa and the frequency of mucosal involvement is somewhat low, whereas multidetector CT (MDCT) is helpful in distinguishing MGC from NMGC.^[7]

The role of imaging is preoperative staging of the disease as well as to determine treatment response.^[8],[9] CECT with oral neutral contrast agent or effervescent granules to make the stomach optimally distended is well-accepted standard protocol. MDCT can definitely show the attenuation value of the primary lesion, infiltration depth, involvement of the surrounding structure, and enhancement patterns with little influence from breathing, heartbeat, and GI peristalsis. Moreover, the MDCT scan can sensitively show calcifications if any.^[10]

We are habituated to see the variable enhancing irregular wall thickening, polypoidal mass with or without surface ulceration, which may be associated with perigastric fat stranding and increased vascularity along with locoregional lymphadenopathy in most of the cases with nonmucinous adenocarcinoma stomach.^[10]

Differentials for MGC on CT to be considered are primary gastric lymphoma and scirrhous adenocarcinoma (signet-ring cell adenocarcinoma).

Primary gastric lymphoma shows diffuse moderately enhancing mural thickening and extensive lateral extension of the tumor due to submucosal spread with extensive locoregional lymphadenopathy (more than adenocarcinoma) without gastric outlet obstruction. Grading of lymphoma is proportionate with severity of gastric wall thickening. A greater thickening may indicate transformation to a high-grade lymphoma.^[11] Between endoscopic ultrasonography (EUS) and CT, EUS is better in the evaluation of parietal extension of tumor while CT better assesses the extra parietal involvement.^[11]

Linitis plastica is classically described in scirrhous adenocarcinoma with diffuse submucosal infiltration with histopathological subtype of signet-ring cell adenocarcinoma.

MGC shows a completely different appearance on CT scan. Here, diffuse wall thickening is seen usually involving a wide segment of the stomach wall due to submucosal spread with a layered enhancement pattern. The wall thickness of MGC was significantly thicker than for nonmucinous gastric cancer (NMGC), which is consistent with the report by Yan et al.^[7] Significant enhancement was noted at innermost layer (mucosa) and no enhancement in middle and outer layer. According to Zhao et al.^[4] and Park et al.,^[12] layered enhancement was the main pattern of MGC, while the most common pattern in NMGC was homogeneous enhancement, followed by heterogeneous enhancement. Both Yuan et al.^[2] and Zhao et al.^[4] concluded that the degree of enhancement of the inner layer in MGC was significantly higher than that of NMGC, while the middle or outer layer in MGC was significantly less enhanced compared to NMGC in portal venous phase. The accuracy (86.1%), sensitivity (83.3%), and specificity (87.2%) of layered enhancement in the diagnosis of MGC are very high. The above findings are consistent with our case.

Depending on the course and advancement of the disease, the amount of mucinous ascites and subsequent scalloping of solid visceral surface occurs in similar fashion like others mucin-producing neoplasm (pseudomyxoma peritonei). It is a single independent poor prognostic factor.^[12]

Punctate, miliary foci of calcification, and easily identified in noncontrast computed tomography (CT) are very characteristic.^[4],[13] Calcification in gastric cancer is a rare finding but when present, they usually associated with mucinous carcinoma. Calcifications had a high specificity (98.7%) in the diagnosis of MGC.^[4] Multiple calcific foci actually develop in extracellular pool of mucin which gives a diagnostic clue.

Mucin pool calcification is distinguished from the circumscribed and patchy calcification seen in benign tumors such as leiomyomata and hemangiomas. Psammomatous calcifications are seen in nonmucin-producing carcinomas, especially in gynecologic serous malignancies. The type of calcification observed on CT imaging of malignancies has been described as dystrophic, metabolic/metastatic, and heterotopic ossification suggesting differences in the pathogenesis of the calcification. Dystrophic calcification is observed with tissue necrosis and also caused by chemoradiotherapy, whereas metabolic calcification occurs with disorders of mineral balance, such as with hyperparathyroidism or uremia, where serum calcium is raised. Heterotopic ossification refers to bone formation in tumors which has been rarely described in well-differentiated primary and metastatic adenocarcinomas.^[14],[15]

Several researches work done for identifying the prognostic factors for MGC but still, it is controversial and unclear. MGC is considered a risk factor of unfavorable outcomes, as compared with NMGC because advanced stage at presentation and predilection for distant and peritoneal metastasis.^[4] The presence of punctate calcification has no role with prognosis.^[2] Distant or lymph nodal metastasis or association with mucinous ascites has got poor prognosis.^[4]

Conclusion

MGC is a rare histological subtype of stomach cancer usually occurred in the elderly with a high grade of malignancy. Layered enhancement patterns and punctate foci of calcifications are characteristic CT features for confident diagnosis. Compared to NMGC, MGC has a thicker gastric wall, larger tumor size, and is more frequently in an advanced stage when discovered. The radiologist should be aware of these classical radiological findings for confident diagnosis as diagnostic sensitivity of MGC by endoscopic biopsy is relatively low.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1.	Hu B, El Hajj N, Sittler S, Lammert N, Barnes R, Meloni-Ehrig A. Gastric cancer: Classification, histology and application of molecular pathology. J Gastrointest Oncol 2012;3:251-61.
2.	Yuan Y, Chen Z, Chen J, Huang W, Peng J, Ye J, et al. Mucinous gastric carcinoma: An update of clinicopathologic features and prognostic value from a retrospective study of clinical series. Int J Clin Exp Pathol 2018;11:813-21.
3.	Isobe T, Hashimoto K, Kizaki J, Matono S, Murakami N, Kinugasa T, et al. Characteristics and prognosis of mucinous gastric carcinoma. Mol Clin Oncol 2015;3:44-50.
4.	Zhao J, Ren G, Cai R, Chen J, Li H, Guo C, et al. Mucinous adenocarcinoma and non-mucinous adenocarcinoma: Differing clinicopathological characteristics and computed tomography features in gastric cancer. Oncotarget 2017;8:45698-709.
5.	Lee NK, Kim S, Kim HS, Jeon TY, Kim GH, Kim DU, et al. Spectrum of mucin-producing neoplastic conditions of the abdomen and pelvis: Cross-sectional imaging evaluation. World J Gastroenterol 2011;17:4757-71.
6.	Choi KS, Suh M. Screening for gastric cancer: The usefulness of endoscopy. Clin Endosc 2014;47:490-6.
7.	Yan C, Zhu ZG, Yan M, Zhang H, Pan ZL, Chen J, et al. Clinicopathological characteristics and computed tomography features of mucinous gastric carcinoma. J Int Med Res 2011;39:291-301.
8.	Altini C, Niccoli Asabella A, Di Palo A, Fanelli M, Ferrari C, Moschetta M, et al. 18F-FDG PET/CT role in staging of gastric carcinomas: Comparison with conventional contrast enhancement computed tomography. Medicine (Baltimore) 2015;94:e864.
9.	Yu T, Wang X, Zhao Z, Liu F, Liu X, Zhao Y, et al. Prediction of T stage in gastric carcinoma by enhanced CT and oral contrast-enhanced ultrasonography. World J Surg Oncol 2015;13:184.
10.	Hallinan JT, Venkatesh SK. Gastric carcinoma: Imaging diagnosis, staging and assessment of treatment response. Cancer Imaging 2013;13:212-27.
11.	Lo Re G, Federica V, Midiri F, Picone D, La Tona G, Galia M, et al. Radiological features of gastrointestinal lymphoma. Gastroenterol Res Pract 2016;2016:2498143.
12.	Park MS, Yu JS, Kim MJ, Yoon SW, Kim SH, Noh TW, et al. Mucinous versus nonmucinous gastric carcinoma: Differentiation with helical CT. Radiology 2002;223:540-6.
13.	Hwang HY, Choi BI, Han JK, Lee DH, Lee BH, Chung KB, et al. Calcified gastric carcinoma: CT findings. Gastrointest Radiol 1992;17:311-5.
14.	Lin YH, Yao W, Fei Q, Wang Y. Gastric cancer with calcifications: A case report. World J Clin Cases 2021;9:8135-41.
15.	Kaneko M, Namisaki T, Takaya H, Mori H, Kitade M, Okura Y, et al. Calcified mucinous adenocarcinoma of the stomach metastatic to the iris: A case report. J Med Case Rep 2019;13:64.