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 Table of Contents  
Year : 2023  |  Volume : 14  |  Issue : 1  |  Page : 62-66

A case report of synchronous primary gastric hodgkin lymphoma and lung adenocarcinoma and literature review

1 Department of Medicine, Faculty of Medicine and Health Sciences, Universiti Malaysia Sarawak, Kota Samarahan, Malaysia
2 Prince Court Medical Centre, Pantai Premier Pathology, Kuala Lumpur, Malaysia

Date of Submission15-Nov-2022
Date of Decision17-Dec-2022
Date of Acceptance18-Dec-2022
Date of Web Publication17-Feb-2023

Correspondence Address:
Dr. Jew Win Kuan
Department of Medicine, Faculty of Medicine and Health Sciences, Universiti Malaysia Sarawak, Kota Samarahan 94300, Sarawak
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/joah.joah_100_22

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We report a rare case of a 58-year-old woman who was initially diagnosed as primary gastric (PG) T-cell non-Hodgkin lymphoma, which later was revised as PG Hodgkin lymphoma (HL) with dissemination to the lung (stage IV). The lung lesion was later found to be lung adenocarcinoma (LA) and the diagnosis was revised again as synchronous primary gastric Hodgkin lymphoma (PGHL) and LA which, to our knowledge, was not reported before. This case illustrated the need of vigilance in the diagnosis of lymphoma at uncommon sites and the clinical challenges in managing synchronous malignancies. The rationale of clinical suspicion, the association between PGHL and Epstein–Barr virus, Helicobacter pylori, and other infections, and synchronous PGHL and LA were discussed.

Keywords: Extranodal, gastric, Hodgkin lymphoma, lung adenocarcinoma, synchronous

How to cite this article:
Kuan JW, Masir N. A case report of synchronous primary gastric hodgkin lymphoma and lung adenocarcinoma and literature review. J Appl Hematol 2023;14:62-6

How to cite this URL:
Kuan JW, Masir N. A case report of synchronous primary gastric hodgkin lymphoma and lung adenocarcinoma and literature review. J Appl Hematol [serial online] 2023 [cited 2023 Jun 4];14:62-6. Available from: https://www.jahjournal.org/text.asp?2023/14/1/62/369838

  Introduction Top

Lymphoma constitutes about 1.2%[1] to 12%[2] of gastric malignancies. Lymphoma commonly presents as a nodal disease, while sometimes it may arise from an extranodal site – the primary extranodal lymphoma (PENL). The definition of PENL is controversial for two reasons. First, the sites to be considered extranodal, for example, some regard spleen and Waldeyer's ring as extranodal. However, gastric is less controversial to be regarded as extranodal. Second, in stages III and IV, it is difficult to differentiate primary nodal disease with the disseminated extranodal site or PENL with lymph nodes (LN) metastasis.[3]

PENL is rare in Hodgkin lymphoma (HL) but more common in non-HL (NHL), about 25% to 35%,[4] in which gastric is the most common,[1] about 3% to 10%.[4] Primary gastric (PG) HL (PGHL) is much rarer than PGNHL which is about 90% to 97%[1],[5],[6],[7],[8] of PG lymphoma. During a PubMed search, we identified 93 studies of PGHL, in which the earliest case report identified was 1946.[9],[10] Of note, Reed–Sternberg cells were described, and HL was emphasized to be unrelated to tuberculosis by Dorothy Mabel Reed Mendenhall in 1902.[11]

Lung cancer is the third most common cancer in women in Malaysia with an age-standardized rate of 5.9[12] and only 3% were diagnosed at stage I.[13]

In this case report, we present a rare case of synchronous PGHL and lung adenocarcinoma (LA) which was diagnosed after a series of events and, to our knowledge, was not reported before.

  Case Report Top

In May 2019, a 58-year-old woman from a neighboring country, nonsmoker and with no known illness, presented with progressive weight loss of 22 kg over a year associated with loss of appetite, nausea, vomiting, and upper abdominal pain for 7 months. Examination revealed hepatomegaly of about 8 cm below the costal margin. Otherwise, there was no fever, night sweats, lymphadenopathy, or splenomegaly. There was no family history of malignancy. Investigation showed hemoglobin – 9.2 g/dL, total white cell – 6.279 × 109/L, platelet – 526.3 × 109/L, erythrocyte sedimentation rate (ESR) – 120 mm/h, albumin – 35 g/L, alkaline phosphatase – 262 U/L (30–120), and gamma-glutamyl transferase – 168 U/L (<50), and positive venereal disease research laboratory and Treponema pallidum hemagglutination. Other blood investigations were unremarkable including lactate dehydrogenase. Computed tomography (CT) abdomen revealed circumferential thickening of the proximal gastric body of about 3.6 cm in length with wall thickness up to 1 cm, enlarged LN at perigastric (extensive, largest 1.6 2 cm × 2.2 cm), coeliac (some, largest 0.7 2 cm × 1.0 cm), and pancreatic head region (one LN, 1.6 2 cm × 3.5 cm). The right lobe of the liver was enlarged with a span of 18.3 cm, likely Riedel's lobe (normal variant).

Because of financial constraints, she did not pursue further investigations. She went back to her country and returned in July 2019 for esophagogastroduodenoscopy (OGDS), which showed a cardia tumor, gastritis at antrum, and positive urease test. The cardia tumor biopsy was reported as gastric T-cell NHL. In view of the rarity of gastric T-cell NHL, the biopsy was sent for second opinion. She was given Helicobacter pylori (HP) treatment (2 weeks of clarithromycin, amoxicillin, and pantoprazole) and intramuscular benzathine penicillin 2.4 MU weekly for 3 weeks.

When the diagnosis of gastric classical HL from the second opinion was known, she refused further treatment because she felt well. She only came for review in October 2019. The repeat OGDS showed disease progression with the increasing number and size of sites involved. The cardia tumor was bigger and extended to the fundus forming a circumferential tumor with a malignant ulcer. The antrum showed a malignant ulcer and a new malignant ulcer at the incisura. The urease test was negative. Positron emission tomography CT (PETCT) scan showed fluorodeoxyglucose (FDG)-avid lesions in the fundus, body, and antrum of the stomach (SUVmax 27.22 at greater curvature, Deauville 5) and intra-abdominal LNs – coalescence of coeliac and gastrohepatic LNs (maximum combined transaxial short axis 2.8 cm, SUVmax 29.49, Deauville 5), and infrapyloric LNs (largest 1.1 cm, SUVmax 14.27, Deauville 5). The liver and marrow FDG uptake was within normal range and distribution. There was also a spiculated lung mass at the superior segment of the right lower lobe (2.6 cm × 2.3 cm, SUVmax 6.02, Deauville 4). The diagnosis of advance stage gastric HL with poor International Prognostic Score (IPS) (Ann Arbor stage IVEB, IPS 4/7 – stage, age, hemoglobin, and albumin) was made. A bone marrow examination was not done. Prephase chemotherapy (vinblastine), followed by ABVD (doxorubicin 25 mg/m2, bleomycin 10 u/m2, vinblastine 6 mg/m2, and dacarbazine 375 mg/m2 on day 1 and 15; at 28-day interval) was given. After four cycles of ABVD, PETCT scan showed complete remission of the stomach and intra-abdominal nodal disease but persistent lung lesion (2.0 cm × 1.9 cm, SUVmax 2.87, Deauville 4). Subsequently, a CT-guided lung biopsy showed moderately differentiated LA. Then, she was unable to come because of the COVID-19 pandemic and the country lockdown policy. At the time of writing, October 2022, she had not come back for further treatment.

Gastric biopsy

They were densely infiltrated by inflammatory infiltrates of lymphocytes, neutrophils, and eosinophils. In addition, scattered large neoplastic cells were seen within the inflammatory infiltrates [Figure 1]a. The neoplastic cells displayed large, bizarre nuclei including bi-and multinucleated cells with prominent nucleoli resembling Hodgkin and Reed–Sternberg cells (HRS cells) [Figure 1]b. Occasional mitotic figures were also seen. Immunohistochemically the neoplastic cells expressed CD30 [Figure 1]c, PAX5 [Figure 1]d, MUM1, and Ki67 (Ki67 was 100% positive in the neoplastic cells). T-cells markers including CD2, CD3, CD4, CD5, CD7, and CD8 highlighted numerous reactive T cells around the neoplastic cells. The neoplastic cells were negative for all T-cell markers as well as for CD20, CD15, CD10, and cytokeratin.
Figure 1: Gastric biopsy. (a) Scattered large neoplastic cells are seen within the inflammatory infiltrates, (b) Higher power show a few Hodgkin cells with large nucleus and prominent nucleoli (arrow), (c) The Hodgkin cells are strongly positive for CD30, and (d) PAX5 highlights two Reed-Sternberg cells (arrow)

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Lung biopsy

The biopsy consisted of two strips of lung tissue which showed fibrotic lung tissue infiltrated by adenocarcinoma with acinar and lepidic patterns. The irregular neoplastic glands and few alveolar spaces were lined by large malignant cells with nuclear hyperchromasia, moderate nuclear pleomorphism, occasional prominent nucleoli, frequent mitoses, and pale eosinophilic cytoplasm. Atypical mucinous cells were seen in areas with lepidic patterns. There was no squamous component. Scanty lymphocytic inflammation was seen in the intervening fibrotic stroma. There were no Hodgkin cells, atypical lymphoid cells, and granulomas seen in the lung tissue. The adenocarcinoma cells expressed cytokeratin (CK) 7 and thyroid transcription factor-1. The cells were negative for CK20.

  Discussion Top


Second hematopathology opinion was pursued because of two reasons. First, gastric T-cell NHL is rare. Although gastric is the most common site for primary GI lymphoma, about 50% to 75%,[14],[15],[16] B cell is much more common, either in nodal or PGNHL, about 87%[5],[7] to 98%[17] of PGNHL. Small intestine involvement is usually seen in primary GI T-cell NHL small intestine (enteropathy-associated T-cell lymphoma, monomorphic epitheliotropic intestinal T-cell lymphoma, natural killer (NK)/T cell, peripheral T-cell lymphoma etc.), while gastric is usually part of the dissemination.

Second, the initial biopsy report stated many eosinophils, neutrophils, and small lymphocytes were seen between the neoplastic cells. A lymphoma could be misdiagnosed when the neoplastic cells were the minority and surrounded by many reactive/background cells. In our case, a diagnosis of classical HL was made after a careful examination of the histomorphology. The HRS cells which constitute the neoplastic component are usually few and scattered and they are found within a dense inflammatory background. The latter which comprises lymphocytes, neutrophils, eosinophils, and histiocytes could be misinterpreted as reactive inflammatory processes if the neoplastic cells are overlooked. The HRS cells can be recognized as large cells displaying mono-or binucleated cells with prominent nucleoli. Eosinophils are a constant finding within the inflammatory infiltrates that may help raise a suspicion of HL. In addition, a full panel of immunohistochemical markers is essential for an accurate diagnosis of HL. The HRS cells express CD30, CD15, and PAX5 with the latter being typically weakly positive. Being a tumor of B-cell origin, the HRS cells may variably express CD20 but the absence of OCT2 and BOB1 helps to differentiate HL from a CD30+ B cell lymphoma. In our case, CD15 is also negative but this does not exclude HL. Another point of interest is the number of T lymphocytes within the inflammatory cells. In HL, T cells constitute the majority of lymphocytes. Perhaps, this had misled to the initial diagnosis of T-cell lymphoma.

The association between infections and Hodgkin lymphoma

Various infections have been reported in association with HL. Epstein–Barr virus (EBV) is associated with many malignancies, in which the more established are HL, NHL, for example, Burkitt lymphoma and extranodal NK/T-cell lymphoma, nasal type, and solid tumors, for example, gastric carcinoma (GC) and nasopharyngeal carcinoma. In HL, EBV involves in the pathogenesis,[18],[19] but its presence, either in histology or blood sample, is not required for the diagnosis. The prevalence of EBV in HL was between 30% and 67% depending on the studied regions.[20] Gastric HL may demonstrate EBV positivity[21],[22],[23],[24],[25] or negativity.[21],[26],[27],[28] We found five case reports of synchronous PGHL/GC,[22],[28],[29],[30],[31] of which two reported EBV status[22],[28] [Table 1]. EBV status in the biopsy was not checked in our case because it is not required for the diagnosis or treatment of HL.
Table 1: Two studies of primary gastric Hodgkin's lymphoma and gastric carcinoma

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The relationship between PGHL and HP is uncertain, unlike PG marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT) lymphoma, which “spontaneous” regression occurs commonly after HP eradication, consolidating the role of HP in the etiology. There was a case of PGHL with positive HP but treatment/progress was not reported[27] and a case with negative HP.[22] HP is also involved in the oncogenesis of gastric adenocarcinoma but not in LA to our knowledge. In our case, “spontaneous” regression did not happen with HP eradication.

We were unsure of the role T. pallidum in the pathogenesis of PGHL but likely minimal. Of note, gastric syphilis is known to mimic gastric lymphoma.[32],[33],[34],[35] The typical description of gastric syphilis, which is chronic gastritis with dense plasmacytic and lymphocytic infiltrates,[34] was not seen in our case. Similarly, gastric cytomegalovirus usually presents as a gastric ulcer, but occasionally as pseudotumor.[36],[37] Finally, tuberculosis would reveal giant cells, typically Langhan's giant cells which might confuse with HRS cells, in the background of inflammatory cells with or without granuloma, and mimic lymphoma.[38],[39]

Synchronous malignancies

Synchronous malignancies (two or more malignancies occur simultaneously) are rare. There were case reports of synchronous PGHL with, for example, GC as discussed above, gastric MALT lymphoma,[23] and gastric diffuse large B-cell lymphoma.[25],[26] This case demonstrated a rare synchronous PGHL/LA, which we believe was not reported before.

Synchronous malignancies post a few clinical challenges. In our opinion, staging and treatment are the most challenging. Accurate staging is needed for prognostication which nowadays affects the treatment approach. Which malignancy should be treated first? Is there treatment that can treat both simultaneously? In our case, the staging of HL was revised from the advance stage (IVEB) with poor IPS (4/7 – stage, age, hemoglobin, and albumin) to the early unfavorable stage (IIEB) with unfavorable factor (elevated ESR, age, and extranodal disease), which means the prognosis changed from 61%[40] to 90%[41] of 5-year overall survival and the number of ABVD cycle changed from 6 to 8–2–4 using PETCT-guided therapy. If we had known the lung lesion is not HL, PETCT would have been repeated after two cycles of ABVD and we would be more certain on the long-term HL outcome. Nonetheless, with the complete remission on PETCT scan post 4th cycle, her prognosis would be good. For her LA, the disease was at an early stage (stage T1cN0M0) and less active with the “neoadjuvant” ABVD. She would have a very good prognosis with treatment. We could not identify a treatment that can treat both PGHL/LA simultaneously. If the diagnosis of synchronous malignancies was known from the beginning, would we have done things differently? Retrospectively, we would have done similarly by treating HL first because early-stage HL has a good prognosis and ABVD is well tolerated generally. PETCT-guided approach for the number of ABVD cycles should be used, while the patient is assessed for fitness of surgical resection of LA and prepares her financial arrangement.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1]

  [Table 1]


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