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Year : 2021  |  Volume : 64  |  Issue : 1  |  Page : 140-144
Burkitt lymphoma with disseminated pleuroperitoneal and visceral lymphomatosis: Autopsy diagnosis of an unusual case

1 Department of Laboratory Sciences and Molecular Medicine, Army Hospital (Research and Referral), New Delhi, India
2 Department of Medical Oncology, Malignant Diseases Treatment Center, Army Hospital (Research and Referral), New Delhi, India
3 Department of Nuclear Medicine, Army Hospital (Research and Referral), New Delhi, India

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Date of Submission16-Feb-2020
Date of Decision23-Feb-2020
Date of Acceptance18-May-2020
Date of Web Publication8-Jan-2021

How to cite this article:
Guleria P, Guleria B, Ahuja A, Chatterjee T, John AR. Burkitt lymphoma with disseminated pleuroperitoneal and visceral lymphomatosis: Autopsy diagnosis of an unusual case. Indian J Pathol Microbiol 2021;64:140-4

How to cite this URL:
Guleria P, Guleria B, Ahuja A, Chatterjee T, John AR. Burkitt lymphoma with disseminated pleuroperitoneal and visceral lymphomatosis: Autopsy diagnosis of an unusual case. Indian J Pathol Microbiol [serial online] 2021 [cited 2022 Jul 2];64:140-4. Available from: https://www.ijpmonline.org/text.asp?2021/64/1/140/306493

   Introduction Top

Burkitt lymphoma (BL) is a highly aggressive lymphoma with a rapid growth rate and cell doubling time of 24–48 h.[1] It occurs commonly in children and immunocompromised hosts as an extra-nodal disease. In adults, it is rare and occurs sporadically with nodal involvement commonly abdominal and sometimes solid organs.[2] However, the involvement of the appendix,[3] gall bladder, peritoneal lymphomatosis, and multi-organ involvement is extremely rare.[1],[4] Moreover, extra-nodal involvement is also an indicator of poor prognosis.[5]

We present a case of BL involving multiple solid organs (gall bladder, appendix, and pancreas), with surface deposits on the liver and peritoneal lymphomatosis who had a rapidly deteriorating clinical course with a fatal outcome and where a definitive diagnosis was established on autopsy.

   Case Description Top

A 51-year-old male, with no known comorbidities, non-smoker, and nonalcoholic, presented with a 1-month history of distention of the abdomen, progressive breathlessness, weight loss, and loss of appetite. Initial evaluation at a peripheral hospital revealed stable vital parameters, bilateral pleural effusion, and ascites. There were no peripheral stigmata of immunocompromised state or hepatosplenomegaly. Relevant hematological and biochemical parameters during hospitalization have been shown in [Table 1]. Radiological investigations were suggestive of chronic liver disease, ascites with multiple peritoneal deposits, bilateral massive pleural effusion, and omental thickening. The pleural fluid analysis showed lymphocyte-predominant exudative effusion along with reactive mesothelial cells. Ascitic fluid was low serum-ascites albumin gradient (SAAG) with high lactate dehydrogenase (LDH) (35,000 U/L). Multiple attempts for body fluid malignant cell identification were inconclusive. An ultrasound-guided peritoneal biopsy was attempted at the peripheral hospital, however, it yielded nonrepresentative tissue. There was a gradual deterioration in liver functions and serially rising levels of LDH. He was transferred to our tertiary care hospital after 3 weeks of illness and in-hospital stay. Further evaluation at our center with whole-body positron emission tomography-computed tomography (PET-CT) scan revealed metabolically active involvement of peritoneal lining, mesentery, and omentum with soft tissue deposits involving right rectus abdominis and fluorodeoxyglucose (FDG) avid cervical and mediastinal lymphadenopathy, irregular pleural and pericardial thickening with gross pleural effusion, ascites, and mild hepatomegaly. His omental biopsy was reattempted under radiological guidance. The individual had a rapidly worsening clinical course with features of multiorgan involvement. His clinical condition deteriorated swiftly, and he succumbed to his aggressive illness on the second day of the omental biopsy, before a definite diagnosis could be established.
Table 1: Hematological and biochemical parameters during illness

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A pathological autopsy was carried out to ascertain the exact cause of death. The postmortem examination confirmed the radiological findings of hemorrhagic effusions, thickened pleura, and diffusely thickened omentum and mesentery. Besides, there were multiple enlarged paratracheal, mediastinal [Figure 1]a, and mesenteric lymph nodes. There were pale yellow fleshy masses attached to the diaphragm bilaterally [Figure 1]b, fleshy deposit on the rectus abdominis muscle [Figure 1]c, and extensive nodular pale yellow fleshy deposits on the mesentery [Figure 1]d. The appendix was grossly enlarged (17 × 2.5 cm) with diffuse thickening of its wall and luminal obliteration [Figure 1]e. There was hepatomegaly with multiple nodular surface deposits with central necrosis in both the lobes [Figure 1]f. The gall bladder was enlarged with a diffusely thickened wall and appeared pale yellowish-white in color [Figure 1]g. The pancreas was also enlarged with a bulky head having diffuse homogenous pale yellowish-white cut surface [Figure 1]h. Sections from all the lymph nodes showed diffuse loss of architecture with the presence of sheets of monomorphic, intermediate to large size lymphoid cells having open chromatin. Admixed among these atypical lymphoid cells were histiocytes, few plasma cells, and some small mature lymphocytes. There was a brisk mitotic activity with karyorrhectic debris. The atypical lymphoid cells were diffusely positive for CD20, CD38, and C-MYC. They were focally positive for CD10 (>40%) and negative for CD3, BCL2, and BCL6. The Ki67 proliferation index was >90%. Sections from the liver deposits, diaphragmatic nodules, deposit over the rectus abdominis muscle, appendix, gall bladder, pancreas, omentum, the surface of the intestines, and pleura showed involvement by this high-grade B-cell lymphoma of Burkitt phenotype [Figure 2]a,[Figure 2]b,[Figure 2]c,[Figure 2]d,[Figure 2]e,[Figure 2]f,[Figure 2]g,[Figure 2]h,[Figure 2]i,[Figure 2]j,[Figure 2]k,[Figure 2]l. Therefore, the overall cause of death was BL with disseminated pleuroperitoneal and visceral lymphomatosis.
Figure 1: Photographs of organs during post mortem examination. (a) Multiple enlarged retrosternal lymph nodes (arrow). (b) Pale yellow fleshy masses on the diaphragm (arrow). (c) Fleshy deposit on rectus abdominis muscle (arrow). (d) Nodular pale yellow fleshy deposits on the mesentery. (e) Enlarged appendix with diffusely thickened wall and obliterated lumen (arrow). (f) Hepatomegaly with nodular surface deposits with central necrosis. (g) Enlarged gall bladder with diffusely thickened wall and pale.yellow appearance. (h) Bulky pancreatic head and homogenous pale-yellowish cut surface (arrow)

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Figure 2: Microphotographs of post mortem specimens. (a) ascitic fluid cytology and (b) lymph node imprint smears show atypical lymphoid cells (Leishman-Giemsa 400×). (c) section from a diaphragmatic nodule, (d) liver nodule, (e) pleura, (f) omentum, (g) pancreas, (h) and rectus abdominis muscle deposit show infiltration by atypical lymphoid cells with brisk mitotic activity and karyorrhectic debris (hematoxylin-eosin 20×). (i) atypical lymphoid cells were diffusely CD20 positive (100×) and (j) CD3 negative (100×). (k) they were also immunopositive for c-MYC (40×). (l) Ki67 proliferation index was >90% (40×)

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   Discussion Top

Sporadic BLs often present as an extra-nodal bulky disease with high tumor burden. They are commonly seen as abdominal masses with the ileocecal region being the most common site.[6] Other commonly involved solid organs include the ovaries, kidneys, and breasts.[7] Our case presented as primarily peritoneal involvement with clinical features of ascites and radiological differentials of carcinomatosis and tuberculosis. Peritoneal involvement by lymphoma is uncommon as the fibrofatty tissue is generally devoid of lymphatics. The route of spread is therefore hypothesized to be from the peritoneal surfaces, via the various ligamentous attachments or through the mesocolon.[5] The radiological differentials include peritoneal carcinomatosis and lymphomatosis which have overlapping features and distinguishing between the two may be difficult.[8],[9] Radiologically, lymphomatosis is associated with the bulky disease with minimal ascites whereas carcinomatosis presents as multiple small nodules with significant ascites.[5] Our patient had omental caking along with massive ascites which could have obscured other specific details. Autopsy reports of similar cases of peritoneal lymphomatosis have been published earlier, wherein one was involvement by T-cell Lymphoma[10] and the other was an aggressive diffuse large B-Cell lymphoma (DLBCL) involving the peritoneum.[11] The offbeat findings of our case in comparison to these reports are the multiple solid organ involvement besides the surface serosal and peritoneal lymphomatosis and no evidence of bulky lymph node disease. Due to the absence of significantly visible lymph node enlargement on repeated radiological investigations, guided-fine-needle aspiration cytology (FNAC) of the lymph nodes was not attempted. Studies have shown that FNACs are extremely useful in diagnosing lymphomas. Besides, it has been seen that lymph nodes other than those in the abdominal region have a lower incidence of non-Hodgkin Lymphomas (NHL) in comparison (incidence of approximately 4%[12] as compared to 28%[13]). The other differentials of a primary peritoneal involvement include mesotheliomas, serous carcinomas, leiomyomatosis, and rarely desmoplastic small round cell tumor. Benign etiologies besides tuberculosis include endometriosis, gliomatosis peritonei, melanosis, and splenosis which may also present with diffuse peritoneal involvement with overlapping radiological features.[14] A tissue biopsy becomes the only way to confirm the diagnosis.

Primary involvement of the appendix[3],[6] or the gall bladder by BL is known, but rare. Simultaneous involvement of the two organs has not been reported in literature yet. The present case involved multiple organs which included the appendix, gall bladder, and pancreas with surface deposits over the liver, intestines, visceral pleura, diaphragm, and the rectus abdominis muscle. The peculiar feature about the appendix in our case was its size which was approximately 17 cm in length with diffusely thickened wall. Similarly, the gall bladder was diffusely enlarged with thickened walls and pale white appearance. Among the NHLs, DLBCL is known to aggressively involve extra-nodal regions. However, BL should be considered over DLBCL when multiple extra-nodal sites are involved.[15] The other sites of primary involvement of the gastrointestinal tract by lymphomas are stomach where mucosa-associated lymphoid tissue lymphoma is common, terminal ileum, jejunum, and colon with mantle cell lymphoma being the most common subtype and follicular lymphoma in the duodenum. Due to the primary involvement of the peritoneal surfaces along with the presence of multiple lymph node enlargements, the application of Dawson's criteria excluded a primary gastrointestinal lymphoma in our case.[16]

The other unusual finding during postmortem examination of our case was the involvement of skeletal muscles (rectus abdominis) and the diaphragms bilaterally. Skeletal muscle involvement by NHL has been seen in 1.5–5% cases of the extra-nodal disease.[17] Moreover, the type of involvement was large nodular deposits instead of diffuse infiltration as seen in the few case reports published earlier. The size of the deposits in the present case was approximately 3 cm in greatest dimension and had firm rubbery consistency.

The antemortem evaluation of the ascitic and pleural fluids were exudative effusions and no malignant cells, however, with raised LDH levels. The examination of the fluids obtained during the autopsy revealed florid involvement by lymphoma cells and even higher LDH levels. The possibility of missing the diagnosis on initial effusion cytology could be low cell counts as well as no initial clinical suspicion of a lymphoma considering the patient's age and clinical presentation. Also, sometimes lymphoma cells resemble activated lymphocytes and a relatively high degree of suspicion is required by the cytopathologist to identify the malignant cells among them.[18]

One important clue in our case that could have risen a suspicion of lymphoma was the increased LDH levels in the effusion samples examined during antemortem evaluation. However, due to the absence of malignant cells on smears, the raised levels were considered to be a feature of the exudative nature of the effusions. A study evaluating pleural effusions in lymphoma patients reveals that pleural fluid LDH levels >128 IU/L are highly suggestive of malignant effusions. Besides, they had found a predominance of exudative effusions with a mononuclear predominant cell population in their cohort of lymphoma patients.[19] This could explain the exudative effusions which we encountered during the initial evaluation of the patient.

BL is a highly chemosensitive malignancy that requires rapid diagnosis for good patient response and outcome. It requires intensive multidrug chemotherapy with adequate central nervous system (CNS) prophylaxis. The chemotherapy regimens used for adults have been adapted from those used in children. The National Comprehensive Cancer Network (NCCN) recommends age-adjusted regimes according to the risk stratification of the patient. The high-risk cases are those with bulky disease, advanced disease, high LDH, and poor performance status with an increased predisposition for CNS relapse and benefit by the inclusion of CNS penetrating drugs in the induction phase. Various regimes followed are CODOX-M (cyclophosphamide, doxorubicin, vincristine with intrathecal methotrexate + cytarabine followed by systemic methotrexate along with rituximab) with or without IVAC (Ifosfamide, Cytarabine, Etoposide, and intrathecal Methotrexate), dose-adjusted EPOCH (etoposide, prednisone, vincristine, cyclophosphamide, doxorubicin + rituximab) or HyperCVAD (cyclophosphamide, vincristine, doxorubicin, and dexamethasone alternating with high-dose methotrexate and cytarabine + rituximab).[20] CALGB 9251 is another option in high-risk patients that encompasses multidrug chemotherapy including CNS penetrating agents with or without CNS irradiation. The lymphoma cells of BL have an extremely swift turn-over with a doubling time of 24–48 h and therefore, a delay in making a diagnosis leads to a catastrophic end. The various deceptive clinical and radiological features including a misleading effusion cytology picture led to rapid disease progression in our case ultimately causing death.

   Conclusion Top

In summary, the aim of presenting this case of BL was to bring about the devious clinical and radiological features associated with this malignancy which baffled all the specialists including clinicians, radiologists, and pathologists equally. It also brings into light the varied manifestations of BL and highlights the importance of not overlooking subtle clinical and biochemical hints which can eventually clinch a diagnosis. This autopsy impresses upon the significance of rapid diagnosis in a fatal disease that is potentially curable.

Disclosure statement

Ethical approval and consent to participate: Not applicable.

Availability of data and material: Data sharing does not apply to this article as no datasets were generated or analyzed during the current study.

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.

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Conflicts of interest

There are no conflicts of interest.

   References Top

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Correspondence Address:
Tathagata Chatterjee
Department of Laboratory Sciences and Molecular Medicine, Army Hospital (Research and Referral), New Delhi - 110 010
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/IJPM.IJPM_128_20

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