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Year : 2018  |  Volume : 61  |  Issue : 3  |  Page : 446-449
Primary follicular lymphoma of disguised as multiple miliary like lesions: A case report and review of literature

1 Department of Pathology, Adichunchanagiri Institute of Medical Sciences, Mandya, Karnataka, India
2 Department of Pathology, Kidwai Cancer Institute, Bengaluru, Karnataka, India

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Date of Web Publication13-Jul-2018


Primary follicular lymphoma (PFL) of gastrointestinal tract (GIT) is rare and account for 1%–3% of non-Hodgkin lymphoma. Within the small intestine, the PFL is more common in jejunum than in the ileum. Due to low prevalence of the disease, the clinical manifestations are not well known, and diagnosis is usually delayed leading to complications. We herein report a case of PFL of GIT who presented with intestinal obstruction and unique gross morphology. Diagnosis was made by morphology and supported by immunohistochemistry.

Keywords: Gastrointestinal tract, lymphoma, non-Hodgkin

How to cite this article:
Amita K, Suma M N, Shankar S V, Premalata C S, Sanjay M. Primary follicular lymphoma of disguised as multiple miliary like lesions: A case report and review of literature. Indian J Pathol Microbiol 2018;61:446-9

How to cite this URL:
Amita K, Suma M N, Shankar S V, Premalata C S, Sanjay M. Primary follicular lymphoma of disguised as multiple miliary like lesions: A case report and review of literature. Indian J Pathol Microbiol [serial online] 2018 [cited 2021 Jul 23];61:446-9. Available from: https://www.ijpmonline.org/text.asp?2018/61/3/446/236594

   Introduction Top

Primary gastrointestinal tract (GIT) lymphomas are rare accounting for 1%–8% of GIT malignancies.[1] Primary follicular lymphoma (PFL) of GIT is a B cell non-Hodgkin lymphoma arising from precursor B cells of germinal center origin. Its incidence is rare, being 1%–3% of all non-Hodgkin lymphoma (NHL).[2]

PFL of GIT does not differ much from its nodal counterparts by morphology and immunohistochemistry (IHC) profile, nevertheless, the former has an excellent prognosis and good overall survival as compared to the later.[2]

The consequence of low prevalence of this entity has made it difficult to recognize the general manifestations of the disease. In addition, most of the time the lesions are asymptomatic, end result being the patients landing in complications at the time of presentation.[3] Herein, we report a rare case of PFL of GIT affecting ileum who presented with intestinal obstruction and discuss the distinct morphology.

   Case Report Top

A 30-year young female presented with a history of acute onset pain in the abdomen and vomiting of 8 days duration. The vomitus contained food particles and she had 7–8 episodes of vomiting per day. There was no history of fever, loose stools, constipation, fever, loss of weight, or burning micturition. There was no history of diabetes mellitus, hypertension, history of tuberculosis, or any other chronic disease. Complete blood count, biochemistry profile, and peripheral smear examination were within normal limits. Ultrasound abdomen revealed a retrocecal appendicitis. Computed tomography (CT) scan of the abdomen revealed a circumferential enhancement in the jejunal bowel loop with associated proximal loop dilation along with mesenteric lymphadenopathy. With these findings, differential diagnoses of infective versus neoplastic etiology were considered. In view of these findings, an emergency laparotomy and segmental resection were done and specimen sent for histopathology.

On gross examination, the segment of small intestine measured 20 cm in length. The lumen was dilated lumen with thinned out wall. A stricture was noted seven cm from one resected end [Figure 1]a. The luminal surface was studded with tiny military such as nodules few were found on the serosal surface [Figure 1]b.
Figure 1: (a) Segment of small bowel with stricture and dilation. (b) Cut surface showing small white miliary such as tubercles on mucosal surface

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The sections from the intestine showed ulcerated mucosa with underlying submucosa and muscularis propria infiltrated by atypical lymphoid cell in follicular pattern. There was striking transmural involvement extending up to the serosa. Centroblasts were <5/high-power field (HPF) [Figure 2]a, [Figure 2]b, [Figure 2]c, [Figure 2]d. A single enlarged mesenteric LN sent along with the main specimen revealed same morphology. Immunohistochemistry performed on both ileal sections, and lymph node revealed similar findings. The neoplastic lymphocytes were positive for CD10, CD 20, bcl 2, and bcl 6. They were negative for CyclinD1, CD5, and CD23. Ki-67 index was low [Figure 3]a, [Figure 3]b, [Figure 3]c, [Figure 3]d. The lymph node sections showed effaced architecture with neoplastic lymphocytes in follicular pattern [Figure 4]a At IHC CD10, CD 20 and bcl 2 were positive, while Ki-67 was negative [Figure 4]b, [Figure 4]b, [Figure 4]c, [Figure 4]d.
Figure 2: Sections from intestine (H and E, ×100) (a) atypical lymphoid infiltrate in lamina propria with mucosal ulceration, (b) nodular architecture, (c) involvement of muscularis propria and (d) Transmural involvement extending up to the serosa

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Figure 3: Sections from intestine (immunohistochemistry, ×100) (a) CD 10 positivity, (b) CD 20 positivity, (c) Bcl 2 positivity and (d) Ki 67 Negativity

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Figure 4: (a) Sections from lymph node A: Effacement of architecture by follicular pattern (Hematoxylin and Eosin, ×100). (b) CD 10 positivity, (c) Bcl 2 positivity and (d) Ki 67 Negativity. (Immunohistochemistry, x100)

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A final diagnosis of follicular lymphoma of small intestine was made.

A thorough workup was done to exclude systemic involvement which included whole-body CT scan, X-ray, and bone marrow examination. They were unremarkable. Hence, a final diagnosis of PFL of small intestine was made. Ann Arbor staging system was stage II E. Since it was a Grade 1 follicular lymphoma as per 2008 WHO classification system, no further treatment was instituted. One and half year after the diagnosis, there has been no evidence of recurrence or metastasis.

   Discussion Top

Follicular lymphoma is a B cell NHL arising from the centrocyte or centroblast with at least a partial follicular pattern. Follicular lymphoma usually involves lymph node and other hematopoietic organs such as spleen, bone marrow, or Waldeyar's ring. Extranodal nonhematopoietic involvement like in the skin, GIT, soft tissue, etc., is rare and usually occurs secondary to the primary nodal lymphomas.[4] Primary FL involving GIT is very rare accounting to 1%–3% of NHL.

Primary GIT FL occurs frequently in middle age and with predilection for females. Most patients are asymptomatic, vague abdominal pain, and vomiting are usual symptoms, while many are diagnosed incidentally at endoscopic biopsy done for some other reasons.[5],[6] Cases presenting with acute obstruction is rare and often occurs in the presence of distal small bowel involvement. Misdraji et al. in their experience of 39 cases of PFL of GIT observed intestinal obstruction as the initial manifestation in five cases.[1] At endoscopy and gross examination of the resected specimens, FL appears as single or multiple polypoidal masses 1–2 cm in size often referred to as lymphomatoid papulosis or as diffuse thickening of the bowel wall or mucosal thickening or ulcerating bulky masses.[4],[6]

In the present case, the gross appearance was unified by the presence of multiple miliary such as tubercles on the mucosa as well as on the serosa associated with stricture formation, which raised suspicion of tuberculosis.

At microscopy, primary FL of GIT does not show any variation from its nodal counterpart. FL needs to be differentiated from other NHL that can involve GIT like extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT), small cell lymphoma, marginal zone lymphoma, immunoproliferative small intestinal disease (IPSID), and a reactive process. Many of these NHL may demonstrate a follicular pattern which may render the morphologic diagnosis difficult. MALT lymphoma frequently exhibits diffuse architecture. MALT lymphoma and IPSID have striking plasmacytic differentiation. The follicles of the follicular lymphoma need to be differentiated from reactive follicles. The follicles of FL are arranged back to back and lack pale and polarized antigenic centers. The cells are monotonous comprising predominantly of centrocytes and varying degree of centroblasts. In indeterminate cases, IHC annihilates accurate diagnosis. MALT lymphoma are positive for CD 20 and CD 79 a. Mantle cell lymphoma shows positivity for CD 5 and cyclin D1 while small cell lymphoma show CD 5 positivity and Cyclin D 1 negativity. Follicular lymphoma is positive for CD 10. Bcl 2 is a useful marker to distinguish follicular lymphoma from reactive follicles, FL being Bcl 2 positive.[4]

The grading of FL has prognostic connotations, with high grade reported to have a relatively bad clinical outcome. The grading is based on the number of centroblast. A three-tier grading system is used as follows, O-5 centroblast/hpf – Grade 1, 6-15 centroblast/hpf – Grade 2, and >15 centroblast/hpf – Grade 3.[4] For grading, ten high-power fields are counted in different follicles. Similarly, proportion of tumor showing nodule formation has influence on survival. Hence, the degree of nodular versus diffuse pattern, the grade including the number of centroblasts and disparity in grades in different fields should to be incorporated in the pathology report. GIT FL express bcr gene which have affinity for the antigens of gut lumina. This shows that they are responsive to the growth-promoting signals from ligands of bcr. This helps to explain the localized nature of the disease.

The etiopathogenesis of FL is complex and consists of genomic aberrations and microenvironment milieu. Apart from the most common t (14,18) genetic alteration, loss of IP 36 and 6q and gain of 7,18 and x have been documented. The genetic alterations in FL is far more complex, a fact attested by the recognition of follicular lymphoma in situ, a true precursor lesion of FL.

The prognosis of FL is excellent and various published studies have advocated the “wait and watch policy” in management. Inspite of rare local invasion, there has been no evidence of metastasis. Nevertheless, in 10%–20% of early stage FL, progression occurs within the first year of diagnosis. In a recent study by Iwamuro et al., authors reported a case of primary FL of GIT which progressed to perigastric lymph node 11 months after the initial diagnosis.[7] The authors also observed the increase levels of interleukin 2 receptor in serum which coincided with the progression. The authors stated that the role of this new tumor marker in predicting the progression of the disease.

   Conclusion Top

We report a rare case of primary follicular lymphoma of GIT with distinct miliary like lesions and stricture formation which was unique to this case. We intend to highlight the need for the clinicians and pathologist to be wary of the possibility of primary Follicular GIT lymphoma, as it demands a specific management protocol. Immunohistochemistry plays a major role in definitive diagnosis and planning appropriate treatment.

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

Nakamura S, Matsumoto T. Gastrointestinal lymphoma: Recent advances in diagnosis and treatment. Digestion 2013;87:182-8.  Back to cited text no. 1
Misdraji J, Harris NL, Hasserjian RP, Lauwers GY, Ferry JA. Primary follicular lymphoma of the gastrointestinal tract. Am J Surg Pathol 2011;35:1255-63.  Back to cited text no. 2
Yaranal PJ, Harish SG, Purushotham B. Primary intestinal lymphoma: A Clinicopathological study. Indian J Cancer 2014;51:306-8.  Back to cited text no. 3
[PUBMED]  [Full text]  
Jaffe ES, Harris NL, Stein H, Vardiman JW, editors. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. Vol. 3. Lyon, France: IARC Press; 2001.  Back to cited text no. 4
Takata K, Okada H, Ohmiya N, Nakamura S, Kitadai Y, Tari A, et al. Primary gastrointestinal follicular lymphoma involving the duodenal second portion is a distinct entity: A multicenter, retrospective analysis in japan. Cancer Sci 2011;102:1532-6.  Back to cited text no. 5
Shia J, Teruya-Feldstein J, Pan D, Hegde A, Klimstra DS, Chaganti RS, et al. Primary follicular lymphoma of the gastrointestinal tract: A clinical and pathologic study of 26 cases. Am J Surg Pathol 2002;26:216-24.  Back to cited text no. 6
Iwamuro M, Takenaka R, Mori A, Fujiki S, Miyake T, Asakura S, et al. Rapidly progressed primary intestinal follicular lymphoma with elevation of soluble interleukin-2 receptor levels. Case Rep Oncol Med 2014;2014:549248.  Back to cited text no. 7

Correspondence Address:
K Amita
Department of Pathology, Adichunchanagiri Institute of Medical Sciences, BG Nagara, Mandya - 571 448, Karnataka
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/IJPM.IJPM_126_17

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This article has been cited by
1 Erratum: Primary follicular lymphoma of disguised as multiple miliary like lesions: A case report and review of literature
Indian Journal of Pathology and Microbiology. 2018; 61(4): 643
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