Small bowel lymphoma on small bowel endoscopic ultrasound: Case presentation and literature review

doi:10.21203/rs.3.rs-3644153/v1

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Small bowel lymphoma on small bowel endoscopic ultrasound: Case presentation and literature review

https://doi.org/10.21203/rs.3.rs-3644153/v1

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Diagnosing small bowel lymphoma is difficult, for which small bowel ultrasound endoscopy can be used effectively. This study summarizes the presentation of small bowel lymphoma on small bowel endoscopic ultrasound. We retrospectively analyzed the clinical features and imaging and endoscopic characteristics of five patients with small bowel lymphoma admitted to the Sixth Affiliated Hospital of Sun Yat-sen University between April and October 2023. A literature review was conducted by searching the PubMed database, Web of Science, and Embase using “small bowel,” “small intestinal,” “endoscopic ultrasound,” and “lymphoma” as search terms with a date range from January 2000 to October 2023. We included five patients (four men and 1 woman) of 48–72 years of age. Enteroscopy indicated ulcerative small bowel lymphoma in two cases and mass-like small bowel lymphoma in three cases. Three cases were surgically treated, and two were treated using chemotherapy. We classified the small bowel endoscopic ultrasound presentation of small bowel lymphoma into two types based on enteroscopic presentation. (1) Limited or diffuse circumferential thickening of the bowel wall with homogeneous hypoechogenicity and loss of its normal layered organization and (2) Thickening of the entire bowel wall but without fusion, presenting as thickening of the muscularis propria.

Health sciences/Diseases

Health sciences/Gastroenterology

small bowel

lymphoma

endoscopic ultrasound

enteroscopy

This study retrospectively analyzed the clinical features, enteroscopic manifestations, small bowel endoscopic ultrasound manifestations, and treatment of five patients with small bowel lymphoma admitted between April and October 2023. The study was approved by the ethics committee of the Sixth Affiliated Hospital, Sun Yat-Sen University (Ethics Number: 2023ZSLYEC-264).

Case 1

A 72-year-old man was admitted due to intermittent black stools for over 1 year.

Double balloon enteroscopy

A bulging, irregular mass of approximately 10 cm in length was found in the distal jejunum. The surface of the mass was covered with white mucus.

Small bowel endoscopic ultrasound

It suggested thickening of the entire bowel wall, fusion and loss of demarcation of bowel wall layers, hypoechoic changes in some areas, and even lower echogenicity inside the hypoechoic areas.

Pathology

Lymphoid cells were diffusely distributed in the mucosal tissues. The cytosol was predominantly small- to medium-sized. Large cells with round or irregular nuclei were observed.

Immunohistochemistry

CK partially punctate (+), CD79α (+), CD20 (-), CD3 (+), CD5 (-), CD21 (-), CD4 (-), CD8 (+), CD56 (+), TIA-1 (+), CD10 (-), CD2 (+), CD30 (-), CD7 (+), PAX-5 (-)v, approximately 80% of tumor cells were Ki-67 (+), Bcl-2 partially (+), Bcl-6(-), Cy clinD1(-), approximately 30% C-myc weak (+), MuM1 partially (+), and EBERs (-). With the immunohistochemistry results, this was considered a case of non-specific peripheral T-cell lymphoma with abnormal expression of CD79α.

Treatment

Surgery

Postoperative pathology indicated that diffuse proliferation of lymphoid cells in the entire bowel wall was seen in the whole layer of the intestinal wall. The cells were monomorphic and medium-sized, with an intermediate amount of cytoplasm and round or oval nuclei, accompanied by necrosis. Epitheliotropic manifestations were observed in some sites. With hematoxylin and eosin (HE) morphology and immunohistochemistry results, the lesion was diagnosed as a highly invasive T-cell lymphoma consistent with monomorphic epitheliotropic intestinal T-cell lymphoma. No tumor involvement was observed in the resection margins.

Immunohistochemistry: CK (-), CD20 (-), CD19 (-), CD3 (+), CD5 (-), CD56 (+), CD8 (+), CD4 (-), Perforin (+), TIA-1 (+), GranzymeB (+), CD30 (-), approximately 80% of tumor cells were Ki-67 (+), and EBERs (-).

Case 2

A 49-year-old man was admitted due to intermittent black stools for half a year.

Double balloon enteroscopy

A longitudinal lamellar ulcer with a thick white coating and mucosa congestion surrounding the ulcer were observed in the proximal ileum.

Ultrasound endoscopy of the small intestine

Thickening of the entire intestinal wall, an indistinct demarcation between the mucosal and submucosal layers in some areas, and localized hypoechoic or hyperechoic changes in the submucosa and muscularis propria.

Treatment

Surgery

Pathology and immunohistochemistry

Many lymphoid cells with a diffuse or nodular distribution were observed in all layers of the intestinal wall, suggesting the possibility of a lymphohematopoietic tumor.

Immunohistochemistry: CD79α (+), CD20 (+), CD3 (-), CD5 (-), CD43 (-), CD21FDC (+), CD10 (-), Bcl-2 (+), Bcl-6 (-), CyclinD1 (+), approximately 5% of tumor cells were Ki-67 (+), MUM1 (-), LEF1 (-), and EBERs (-). Considering both HE morphology and immunohistochemistry results, the diagnosis was mucosa-associated tissue lymphoma.

Case 3

A 68-year-old woman was admitted due to recurrent abdominal pain for over 1 year

Double balloon enteroscopy

A bulging, circumferential mass of approximately 15 cm long with a white coating and congestion were observed in the proximal ileum.

Ultrasound endoscopy of the small intestine

There was thickening of the entire bowel wall, fusion of bowel wall layers, indistinct demarcation between the submucosa and muscularis propria, hypoechoic changes in some areas of the submucosa, and even lower echogenicity inside the hypoechoic areas within muscularis propria.

Pathology and immunohistochemistry

Infiltration of heterogeneous lymphoid cells with occasional mitotic figures was observed. HE morphology and immunohistochemistry findings showed that the lesion was consistent with aggressive B-cell lymphoma and was suggestive of an anaplastic variant of diffuse large B-cell lymphoma. CD20 (+), CD21FDC (+), CD3 (-), CD5 (-), CD79α (-), Ki-67 has a high proliferation index, Bcl-2 (-), Bcl-6 (+), CD10 (-), CD23 (-), C-myc (+), CyclinD1 (-), and MUM-1 (-).

Treatment

Rituximab + cyclophosphamide + doxorubicin + vincristine + prednisone regimen

Case 4

A 48-year-old man was admitted due to black stools for 6 months

Double balloon enteroscopy

An irregular, elevated, circumferential mass of approximately 10 cm long with a yellowish-white coating was observed.

Ultrasound endoscopy of the small intestine

The entire bowel wall was thickened, and there was fusion and loss of demarcation of bowel wall layers.

Pathology and immunohistochemistry

In the small bowel mucosa tissue, large, markedly heterogeneous lymphoid cells were observed to be diffusely distributed in sheets. CD3 (+), CD5 (-), CD2 (-), CD7 (+), CD4 (-), CD8 (+), CD56 (+), TIA-1 (+), GRB (+), CD21 (-), CD20 (-), CD79α (-), approximately 70% of tumor cells were Ki-67 (+), and CD30 (-). All these, with the immunohistochemistry results, showed that the lesion was consistent with T-cell lymphoma.

Treatment

Surgery

Case 5

A 51-year-old man was admitted due to black stools for 1 year

Double balloon enteroscopy

Multiple irregular, depressed, debris-covered ulcers were observed, starting from the distal duodenum to the proximal jejunum.

Ultrasound endoscopy of the small intestine

The entire bowel wall was thickened, predominantly in the muscularis propria.

Pathology and immunohistochemistry

In the small bowel mucosa tissue, it indicated atrophied crypts, blunted villi, and highly heterogeneous lymphoid cells in the interstitium. Some nucleoli and apoptosis were observed. CD3 (+), CD5 (-), approximately 80% of tumor cells were Ki-67 (+), CD20 (-), CD79a (+), TIA-1 (+), GRB (-), CD56 (-), CD8 (-), CD7 (+), CD2 (+), D4 (+), ALK (-), and CD30 (-). The immunohistochemistry results were consistent with T-cell-derived lymphoma. Therefore, peripheral T-cell lymphoma was considered highly probable.

Treatment

Vincristine + cyclophosphamide + epirubicin + dexamethasone + etoposide regimen + tucidinostat

A literature review was conducted by searching the PubMed database, Web of Science, and Embase using “small bowel,” “small intestinal,” “endoscopic ultrasound,” and “lymphoma” as search terms with a date range from January 2000 to October 2023. [1,2]Two papers describing five cases were retrieved (Table 1).

Table 1

Literature reports of presentation of small bowel lymphoma on small bowel endoscopic ultrasound
Sex	Age	Reason for enteroscopy	Endoscopic ultrasound presentation	Disease	Treatment
Male	81	Gastrointestinal bleeding of unknown cause	Homogeneous, hypoechoic	Malignant lymphoma	Chemotherapy
Male	50	Other examinations suggestive of small bowel lesions	Homogeneous, hypoechoic	Malignant lymphoma	Chemotherapy
Male	67	Anemia, bowel obstruction	Necrosis of the bowel wall	Malignant lymphoma	Chemotherapy
Female	46	Imaging examination, suggestive of small bowel lesions	Homogeneous, hypoechoic, originating from mucosa	Diffuse large B-cell lymphoma	/
Male	49	Imaging examination, suggestive of small bowel lesions	Homogeneous, hypoechoic	Follicular lymphoma	/

Primary small intestinal lymphomas are malignant tumors originating from the lymphoid tissue of the intestinal lamina propria and submucosa and account for 19–38% of small bowel malignancies and 20–30% of all primary gastrointestinal lymphomas. [3] Its early symptoms are insidious and lack specificity, and the treatment plan and prognosis are directly dependent on the accuracy of clinical staging and whether it is diagnosed at an early stage. Thus, preoperative diagnosis is essential.

Intestinal ultrasound, small bowel computed tomography (CT), small bowel magnetic resonance imaging (MRI), and other imaging examinations may lack accuracy in localization. They may be affected by gas in the intestinal lumen, echo signal attenuation, intestinal peristalsis, and water consumption by the patient. Small bowel endoscopic ultrasound is performed through the lumen of the intestinal tract. The ultrasound probe directly contacts the lesion, minimizing their distance from each other, thereby preventing interference from intestinal gas, reducing echo signal attenuation, and increasing resolution, thus yielding the histological characteristics of the various layers of the bowel and producing endoscopic ultrasound images of the surrounding organs. [4]

Compiling the experience at our center and our literature review, we classify the small bowel endoscopic ultrasound presentation of small bowel lymphoma into two types based on enteroscopic presentation. (1) Limited or diffuse circumferential thickening of the bowel wall with homogeneous hypoechogenicity and loss of its normal layered organization, as observed in cases 1, 3, and 4. (2) Thickening of the entire bowel wall but without fusion, presenting as thickening of the muscularis propria, as observed in cases 2 and 5. Differential diagnoses include other small bowel diseases such as small bowel mesenchymal tumors, adenocarcinoma, Crohn’s disease, and gastrointestinal tuberculosis.

We advanced our center’s experience and partially summarized the small bowel endoscopic ultrasound presentation of small bowel disease as follows. Small bowel mesenchymal tumors are often masses that grow toward the lumen and outward and are large in volume. Larger tumors are often accompanied by hemorrhage, necrosis, or cystic degeneration. On small bowel endoscopic ultrasound, they present as hypoechoic changes with clear borders, often appearing round and originating from the muscularis propria in most cases. However, they can also originate from the mucosa. Small bowel adenocarcinoma lesions are often more limited, tending to develop in the proximal small bowel, with local stiffness of the bowel wall and narrowing of the lumen, often accompanied by enlarged lymph nodes surrounding the lesion. In the presence of invasive blood vessels, the strong echogenicity of the fat surrounding the blood vessels disappears. When the blood vessels are partially or completely encapsulated by the mass, necrosis of the bowel wall layers is observed on small bowel endoscopic ultrasound as heterogeneous hypoechogenicity and rupture of the serosa. The small bowel endoscopic ultrasound presentation of Crohn’s disease involves different degrees of thickening in different layers of the bowel wall, predominantly in the submucosa and the muscularis propria.

In addition, the submucosa may exhibit slight hyperechoic or hypoechoic changes. Layers can be distinguished, but the demarcation is poor. The structure of the submucosa and the muscularis propria is lost at the ulcer site. Intestinal tuberculosis presents on small bowel endoscopic ultrasound as the absence of the mucosa at the ulcer site; thickening of the bowel wall surrounding the lesion, predominantly the muscularis propria; and thinning of the submucosa with decreased echogenicity.

There are few cases of small bowel lymphoma diagnosed by small bowel endoscopic ultrasound described in the literature, and we expect future data to confirm the results of the present study.

Funding

None.

Acknowledgments

None.

Author contributions

Author contributions: LZC study design, data collection,data analysis, writing of the manuscript; responsible for the integrity of the work from inception to published article. HZC: study design,data collection, data analysis.PB: patient recruitment, data collection. data collection.XT: data collection, data analysis. LM: pathological analysis, data collection. GQ: patient recruitment, data collection.All authors approved the final version of the manuscript.

Competing interests

The authors declare no competing interests.

Data availability

The data that support the findings of this study are available on requests from the corresponding author.

Fukumoto, A. et al. Usefulness of EUS with double-balloon enteroscopy for diagnosis of small-bowel diseases. Gastrointest. Endosc. 65, 412–420 (2007). https://doi.org/10.1016/j.gie.2006.08.045 [2] Wada, M. et al. Endoscopic ultrasound with double-balloon endoscopy in the evaluation of small-bowel disease. Surg. Endosc. 28, 2428–2436 (2014). [3] Nakamura, S. et al. A clinicopathologic study of primary small intestine lymphoma: prognostic significance of mucosa-associated lymphoid tissue-derived lymphoma. Cancer. 88, 286–294 (2000). [4] Deprez, P. H. et al. Endoscopic management of subepithelial lesions including neuroendocrine neoplasms: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 54, 412–429 (2022).

No competing interests reported.

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Small bowel lymphoma on small bowel endoscopic ultrasound: Case presentation and literature review

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