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. 2020 Aug 6;3(5):e1264. doi: 10.1002/cnr2.1264

Primary diffuse large B cell lymphoma of Uterine Cervix: Treatment outcomes of a rare entity with literature review

Jayant Sastri Goda 1,✉, Utpal Gaikwad 1, Anand Narayan 1, Durva Kurkure 1, Subhash Yadav 1, Nehal Khanna 1, Hasmukh Jain 1, Bhausaheb Bagal 1, Sridhar Epari 1, Priya Singh 1, Manju Sengar 1, Siddharth Laskar 1
PMCID: PMC7941478  PMID: 32761885

Abstract

Background

Primary lymphomas involving the female genital tract are rare, and those arising from cervix are extremely uncommon. They are often misdiagnosed because of their rarity.

Methods and cases

The treatment and clinical outcomes of the four cases treated at our institution were compared with the previously published studies. Written informed consent was taken. We highlight four cases of primary diffuse large B‐cell lymphoma of cervix treated at our institution with immunochemotherapy and radiotherapy. The mean age was 50 years (range, 39‐62 years). Three patients had stage I disease while one had stage II disease. All the patients were in complete remission following treatment with immunochemotherapy and radiation therapy. The average disease free survival was 20 months (range, 8‐43 months). None of the patients had any local or systemic relapse.

Conclusion

These cases highlight the physicians to be aware of this entity as their management, natural history and prognosis is completely different from squamous carcinomas of the cervix. Surgery should not be attempted in these patients. Immunochemotherapy and radiotherapy results in favorable clinical outcomes.

Keywords: cervix, Immunochemotherapy, lymphoma, primary, radiation

1. INTRODUCTION

The estimated global incidence of non‐Hodgkin's lymphoma (NHL) is 3%. 1 Lymph node involvement is commonly observed, although primary extranodal disease could be the only site of presentation in a minority of patients. Only 15% are extranodal where the gastrointestinal tract is the most frequent site of extranodal involvement. Only 0.5% to 1% of all NHL cases arise from female genital tract which includes the ovaries, uterus cervix, vagina or vulva. The criteria for diagnosing a case of primary extranodal lymphoma of the uterus was initially given by Fox & More in 1965. 2 The criteria included if (a) the disease to be confined to uterus; (b) staging investigation should not reveal involvement of systemic disease; (c) The peripheral blood examination should not show any evidence of leukemia; and (d) there should be a lag time of several months between the genital tract lymphoma and appearance of secondary lymphomatous deposits at other sites. 2

The commonest histology of primary lymphomas of the Uterine Cervix (LUCx) is diffuse large B‐cell lymphoma (DLBL) accounting for more than 70% cases. 3 , 4 Others histologies include follicular lymphoma (16%), Burkitt's, Mucosa associated lymphoid tissue (MALT) lymphoma and T‐cell NHL(3%‐5%). 5 Lymphomas of the female genital tract are more commonly a secondary manifestation of the disseminated disease and can rarely be the primary manifestation. The most frequent site of primary involvement is the ovary. 6 LUCx is quite rare accounting for only 0.008% of all cervical tumors and 2% of all female extranodal lymphomas. 7 , 8 Because of the rarity of disease, there are no established treatment protocols for these patients. A conservative approach of combined modality treatment using combination immunochemotherapy followed by consolidative radiotherapy has been the widely practiced treatment. However, there are a few discrete reports of radical surgery followed by chemotherapy for these patients. 9 , 10 , 11 , 12 , 13

The aim of the present study was to describe the four cases of primary diffuse large B‐cell lymphoma of the cervix which were managed at a tertiary care cancer center with conservative multi‐disciplinary approach consisting of immunochemotherapy and radiotherapy and to systematically review the english literature regarding various treatment approaches, their treatment outcomes and prognosis of primary aggressive B‐cell non‐Hodgkin's lymphoma of the cervix.

2. DESCRIPTION OF CASES

2.1. Case 1

A 52 years‐old postmenopausal lady, presented with complaints of bleeding per vagina since 2 months. There was no history of B symptoms (fever, weight loss, night sweats). Examination revealed a large growth involving both lips of cervix. Histology showed an infiltrative tumor arranged in a diffuse growth pattern comprising of monomorphic dyscohesive large cells with fine and coarse nuclear chromatin, brisk mitosis and moderate eosinophilic cytoplasm. On immunohistochemistry, these atypical large cells were diffusely positive for CD20 and CD10 with a high proliferation index (Ki‐67 index) of approximately 80%. Mum‐1 (multiple myeloma oncogene 1) and Bcl‐6 (B‐cell lymphoma‐6) were negative in this case. Thus, presence of dyscohesive large cell with CD20 and CD10 (germinal center marker) positivity confirmed Germinal Center type (GC) DLBL (Figure 1A‐F). Staging Positron Emission Tomography (PET) showed a FDG avid soft tissue mass involving cervix. Based on the imaging, she was staged as Stage IE according to Ann Arbor system. She received combination chemotherapy R‐CHOP three weekly (Rituximab, cyclophosphamide, adriyamycin and prednisolone) for 6 cycles. After completion of chemotherapy, she received involved site radiotherapy (ISRT) to a dose of 45 Gy/25 fractions/5 weeks using 3DCRT technique (Figure 2A‐D). Post therapy, she is disease free at 18 months follow‐up Table 1.

FIGURE 1.

FIGURE 1

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A, Scanner view (HE40x)—Histology showing diffuse infiltration by blue cells and hemorrhage. B, Low power (HE100x)—Diffuse infiltration by monomorphic dyscohesive atypical lymphoid cells in the cervical stroma. C, High power (HE400x)—Large atypical lymphoid cells arranged in sheets with apoptosis and mitosis (black arrow). D, Immunohistochemistry (400x)—Weak positivity for CD10. E, Immunohistochemistry (400x)—Diffuse positivity for CD20 delineating a B cell phenotype. F, Immunohistochemistry (400x)—shows high Ki67 index, approximately 80%

FIGURE 2.

FIGURE 2

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A, Digitally reconstructed radiograph (DRR) showing the prescribed radiation dose (in green) to cervix and paracervical tissue. B, Axial view of the pelvis showing the prescribed radiation dose wash with four field beam arrangement using 3D conformal radiotherapy and sparing of bilateral femoral heads. C, Coronal view of the pelvis showing the prescribed radiation dose wash covering the target volume. D, Sagittal view of the pelvis showing the prescribed radiation dose washes covering the target volume and sparing of the rectum behind

TABLE 1.

Patient and treatment Characteristics of primary non‐Hodgkin's lymphomas of the uterine cervix

Characteristics Case 1 Case 2 Case 3 Case 4
Age (y) 52 50 39 62
Type of symptoms Post‐menopausal bleeding Post‐menopausal bleeding Foul smelling discharge Post‐menopausal bleeding
Duration of symptoms (months) 2 − 9 5
Tumor size 6 × 6 cm 3 × 3cm 8 × 7 cm 6 × 5 cm
Immunohistochemistry
CD20 + + + +
CD10 + + − −
MUM1 − − − +
BCL6 Not done Not done Not done −
MIB LI 70%‐80% 70%–80% 50%‐60% Not done
Molecular subtype (by Hans Algorithm) GCB type GCB type Non GCB type Non GCB type
PET SUVmax 13.6 6.59 26.7 Not available a
Bone marrow Negative Negative Negative Negative
Stage (Ann Arbor) IAE IE IAEX IIAE
Treatment R‐CHOP x 6 + ISRT by 3DCRT R‐CHOP x 6 + IFRT TO PELVIS BY 3DCRT R‐CHOP x 6 + ISRT to cervix + pelvic nodes by IMRT R‐CEOP x 6 + IFRT to pelvis by 4 field technique
RT dose 45Gy/25 Fractions RT dose 45Gy/25 Fractions RT dose 45Gy/25 Fractions RT dose 45Gy/25 Fractions RT dose 45Gy/25 Fractions
Response Complete metabolic response Complete metabolic response Complete metabolic response

Complete Morphological

response
Follow up 18 mo 43 mo 8 mo 10 mo
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Abbreviations: C, cyclophosphamide; E, etoposide; GCB, germinal center B cell; H, adriamycin; O, vincristine; P, Prednisalone; PET: positron emission tomography: R, rituximab; SUV, standardized uptake value; X, bulky disease.

a

This patient underwent a staging Contrast CT scan of the neck, thorax, abdomen & pelvis.

2.2. Case 2

A 50 year‐old lady presented with postmenopausal bleeding. She had no history of B symptoms. Biopsy and histomrphology revealed DLBL of cervix. Staging PET/CT Scan showed a bulky cervix with FDG uptake. She was treated with 6 cycles of R‐CHOP followed by IFRT to cervix and pelvic nodes to a dose of 45 Gy/25 fractions/5 weeks using Three Dimensional Conformal Radiotherapy (3DCRT) technique. Post therapy, she is locally controlled at 43 months Table 1.

2.3. Case 3

A 39 year‐old premenopausal lady presented with post coital foul smelling discharge. Vaginal examination revealed a lesion in the posterior lip of the cervix extending into the right wall of vagina. Magnetic Resonance Imaging (MRI) scan showed a bulky cervical mass involving the cervix, upper third of the vagina as well as lower uterine segment. Histopathology revealed DLBL of the cervix. Staging PET revealed FDG avid soft tissue mass with a SUV max of 26.7 (Figure 3A‐G). She was planned for R‐CHOP regimen. Interim response PET showed complete metabolic response (Figure 4A‐C). The patient received 6 cycles of chemotherapy followed by radiotherapy(ISRT) to cervix and paracervical tissues to a dose of 45 Gy/25 fractions. Post therapy she is disease free for 8 months Table 1.

FIGURE 3.

FIGURE 3

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A, Maximum intensity projection of the staging PET scan showing increased uptake in the uterine cervix with no systemic spread of disease. (B‐E) Axial sections of the pelvis showing the bulky cervix with increased FDG uptake on PET scan and the corresponding sections on CT scan shows heterogenous mass. F, Axial sections of the T2W MRI sequence of the pelvis showing a heterogenous T2 dark lesion in the region of uterine cervix. G, Sagittal sections of the T2W MRI sequence of the pelvis showing a heterogenous T2 dark lesion in the region of uterine cervix

FIGURE 4.

FIGURE 4

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A. Maximum intensity projection of the response PET scan done after 4 cycles of R‐CHOP chemotherapy showing no uptake in the region of the uterine cervix. (B, C) Axial sections of the pelvis showing a normal cervix with no FDG uptake on PET scan indicating a complete response to immunochemotherapy (Deauville's 1) and the corresponding sections on CT scan shows a healed cervix

2.4. Case 4

A 62 year‐old postmenopausal lady presented with bleeding per vagina of 5 months duration. Vaginal examination revealed a soft mass in cervix. Histology showed a similar tumor as described in case 1 with atypical large cells arranged in diffuse sheets. These cells were positive for CD20, Bcl‐6 and MUM‐1 and were negative for CD10. This immunophenotype of large cells (MUM‐1+, Bcl‐6+, CD10−) is compatible with DLBL ‐ Non GC type (Figure 5A‐F). A staging CT of the neck, thorax, abdomen & pelvis showed disease localized to cervix and paracervical nodes. Biopsy of the cervix mass showed a DLBL positive for CD20. She received 6 cycles of R‐CEOP followed by IFRT 45 Gy/25 fractions. Patient achieved complete response (CR) to therapy and is in remission both clinically and radiologically at 10 months Table 1.

FIGURE 5.

FIGURE 5

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A, Low power (HE200x)—Large atypical lymphoid cells arranged in diffuse sheets. B, High power (HE400x)—Sheets of large atypical lymphoid cells. C, Immunohistochemistry (400x)—These atypical large cells were diffusely positive for CD20. D, Immunohistochemistry (400x)—These atypical large cells were diffusely positive MUM‐1. E, Immunohistochemistry (400x)—Tumor cells showing diffusely positivity with Bcl‐6. F, Immunohistochemistry (400x)—Tumor cells were negative for CD10

3. DISCUSSION

In this report we have reviewed the existing literature on the management of primary diffuse large B‐cell Lymphoma of Uterine Cervix (LUCx), pertaining to its management and the outcomes. Cervix involvement as a part of multiorgan disease is more common than primary lymphoma of uterine cervix. As in our case series, patients present as early stage disease (stage I and stage II account for 60%). 5 Median age of presentation is fourth to fifth decade, and often misdiagnosed as carcinoma uterine cervix. 5 The mean age of our patients was 50 years (range, 39‐62 years). All the patients were treated with immunochemotherapy followed by consolidation radiotherapy which is now the standard of care for extranodal lymphomas. All the four patients were in complete remission after chemotherapy and consolidation radiotherapy and are disease free on long‐term follow‐up. We did a bibliographic search on Medline database from 2003 till date on primary DLBL of the cervix with treatment and outcomes and found 37 cases of LUCx. Subsequently, results of the studies were examined. We recorded the patient's oncological, treatment and efficacy data (Table 2). Literature revealed that majority of the patients (46%) received chemotherapy with CHOP ± Rituximab while 30% patients underwent surgery in the form of total abdominal hysterectomy which was either upfront or after chemotherapy. Only 24% patients received chemotherapy followed by consolidation radiotherapy. None of the patients received definitive radiotherapy alone. Till 2008, all the patients were treated with CHOP therapy alone with consolidation RT based on the earlier trials. 31 However with overwhelming evidence of efficacy of rituximab (monoclonal anti CD‐20 antibody) in DLBL, from various trials, 32 , 33 , 34 rituximab with CHOP therapy has now become the standard of care, hence from 2009 onwards all the patients received R‐CHOP therapy (Table 2). Patients who received immunochemotherapy with R‐CHOP regimen attained CR and enjoyed long term remission. However, two patients had partial response (chemotherapy alone:1 & surgery alone:1). One patient relapsed after surgery but was successfully salvaged with high dose chemotherapy and bone marrow transplant.

TABLE 2.

Literature review of primary extranodal diffuse large B cell lymphoma of the cervix: Therapeutic outcomes of surgery and/or chemo immunotherapy with radiotherapy

Author (Ref) Stage No of cases Treatment Follow up (months) Response (recurrence/death) DFS (months)
Szantho et al 9 IE 1 CHOP f/b TAH BSO BPLND 60 CR 0/0 60
Heredia et al 14 IE 1 CHOP f/b pelvic radiotherapy 60 CR 0/0 60
IIE 1 m‐CHOP + pelvic RT f/b radical hysterectomy and B/L lymph node dissection 15 CR 15
Dursun et al 10 IE 1 TAH+ BSO f/b CHOP 19 CR 0/0 19
1 CHOP 22 CR 22
Gonzalez‐Cejudo et al 11 IE 1 TAH+ BSO f/b chemotherapy 12 CR 0/0 12
Frey et al 12 IIE 3

TAH+ BSO f/b chemotherapy in 2pts

Chemotherapy f/b TAH + BSO in 1 pt

 15‐38 CR 1/0 a 6‐38
Signorelli et al 13 IE‐IIIE 5 CHOP (6‐10 cycles) d 38‐168 CR 0/0 38–168
IE,IIE 4 TAH + BSO 48‐228 PR b 0/0 48‐228
Ab Hamid et al 8 IE 1 CHOP — PR c ‐ —
Okudaira et al 15 IIE 1 CHOP f/b IFRT 60 CR 0/0 60
Baijal et al 16 IE 1 R‐CHOP f/b IFRT 15 CR 0/0 15
Parva et al 17 IEA 1 R‐CHOP 72 CR 0/0 72
Upanal et al 18 IEA 1 RCHOP f/b IFRT 20 CR 0/0 20
IIEA 1 RCHOP f/b IFRT 19 CR 19
Binesh et al 19 IE 1 RCHOP 05 CR 0/1 05
Parnis et al 20 IE 1 RCHOP f/b IFRT 12 CR 0/0 17
Bull et al 21 IIE 1 RCHOP — CR 0/0 —
Hashimoto et al 22 IIEA 1 RCHOPX8 — CR 0/0
Groszman et al 23 IIE 1 R CHOP 12 CR 0/0 12
Igwe et al 24 IIE 1 R‐CHOP 05 CR 0/0 05
Mendato et al 25 IVEA 1 R‐CHOP 24 CR 0/0 24
Singh et al 26 IE 2 R‐CHOP + IFRT 60 CR 0/0 60
R‐CHOP + IFRT 36 CR 0/0 36
Zhou et al 27 IE 1 R‐CHOP — CR 0/0 01
Sharma et al 28 IIE 1 R‐CHOP+ IT methotrexate + IFRT 01 CR 0/0 01
Regalo et al 29 IIE 1 R‐COP 45 CR 0/0 45
Cubo et al 30 IE 1 R‐CHOP 24 CR 0/0 24
Present study IE 4 R‐CHOP/R‐CEOP f/b RT 8–43 CR 0/0 8–43
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Abbreviations: BPLND, bilateral pelvic lymph node dissection; CR, complete response; DFS, disease free survival.IFRT, involved field radiotherapy; R‐CHOP, rituximab with cyclophosphamide, adriamycin, vincristine, prednisalone; TAH + BSO, total abdominal hysterectomy with bilateral salpingo‐oophorectomy.

a

1 patient who relapsed underwent bone marrow transplant after high dose chemotherapy.

b

Four patients who had partial response post TAH + BSO underwent CHOP chemotherapy and went into remission.

c

Patient underwent CT scan during follow up response assessment scan.

d

Two patients underwent surgery after chemotherapy.

Since LUCx is a rare disease, there is paucity of literature regarding the optimal treatment approach with no consensus among treating physicians due to lack of prospective studies to ascertain the best approach to therapy. On histomorphology, LUCx can be confused with squamous cell carcinoma, where the tumor cells are usually cohesive, dysplastic and show positivity for squamous epithelial markers (p40 and p63) by immunohistochemistry. Other differential includes a florid chronic cervicitis. However, they have a mixed population of mature and reactive lymphoid cells along with plasma cells, thus excluding the possibility of lymphoma. Therefore, awareness of this pathological entity by the clinicians is of utmost importance as the management of LUCx is different from epithelial or stromal tumors of the cervix as the treatment paradigm is based on conservative multimodality therapy of immunochemotherapy with or without radiotherapy.

Lymphomas are considered to be chemo and radiosensitive tumors 35 therefore, role of surgery is limited, but given that these patients are initially seen by a gynecologist, it is not uncommon for the tumors to be surgically excised. Extrapolating the data from nodal DLBL, 32 , 33 , 34 the present‐day approach is to treat these patients with combined rituximab and CHOP regimen followed by consolidation radiotherapy. Such an approach has resulted in a 5‐year survival of approximately 80%. 36 In our series, all the patients were treated with R‐CHOP/R‐CEOP regimen for 6 cycles followed by consolidation RT to cervix and the para‐cervical nodes (Table 1).

Prognosis of female genital lymphomas in general and LUCx in particular has been described to be poorer than nodal lymphomas. 5 , 37 However, when diagnosed at early stage the prognosis is excellent. 14 , 38 The importance of diagnosing the disease at an early stage is therefore of paramount importance especially in low and middle income countries as these patients are initially screened in the gynecology outpatient clinics whose first index of suspicion would be squamous cell carcinoma thereby delaying standard staging procedures and ultimately the treatment which may have a bearing on final the clinical outcome. Gynecologists should always be aware of this disease entity and work closely with other specialists for early diagnosis, staging and initiation of therapy.

Based on the documented outcomes with various modalities and our experience of four patients, we would like to suggest multimodality approach consisting of 4 to 6 cycles of R‐CHOP followed by radiotherapy to the cervix and paracervical tissue using conformal techniques for managing LUCx.

4. CONCLUSION

LUCx is rare entity. Patients treated conservatively with immuno‐chemotherapy and radiotherapy have excellent survival as observed in our patient cohort. Clinically these lesions can be misdiagnosed as they appear similar to more common squamous carcinomas hence primary physicians should be aware of this entity as timely diagnosis, complete staging and conservative management improves clinical outcome.

CONFLICT OF INTEREST

The authors declare no conflicts of interest.

AUTHOR CONTRIBUTIONS

Jayant Sastri Goda: Conceptualization; data curation; formal analysis; funding acquisition; investigation; methodology; supervision; validation; visualization; writing‐original draft; writing‐review and editing. Utpal Gaikwad: Data curation; investigation; methodology. Anand Narayan: Data curation; methodology; resources; visualization. Durva Kurkure: Data curation; methodology; writing‐original draft. Subhash Yadav: Data curation; methodology. Nehal Khanna: Methodology; validation; writing‐review and editing. Hasmukh Jain: Methodology; writing‐review and editing. Bhausaheb Bagal: Investigation; methodology; writing‐review and editing. Sridhar Epari: Formal analysis; methodology; resources; supervision. Priya Singh: Data curation; methodology; resources; visualization. Manju Sengar: Conceptualization; formal analysis; investigation; writing‐review and editing. Siddhartha Laskar: Writing‐review and editing.

ETHICAL STATEMENT

Institutional ethics approval was taken prior to submitting the manuscript. The corresponding author had taken written informed consent from the subjects prior to conduct of the study and analysis.

ACKNOWLEDGEMENT

We acknowledge the generous funding from the intramural grants committee of Tata Memorial Centre and the Department of Science & technology, science and engineering board (DST‐SERB).

Goda JS, Gaikwad U, Narayan A, et al. Primary diffuse large B cell lymphoma of Uterine Cervix: Treatment outcomes of a rare entity with literature review. Cancer Reports. 2020;3:e1264. 10.1002/cnr2.1264

Funding information Science & technology, science and engineering board (DST‐SERB)., Grant/Award Number: EMR/2016/007782; Tata Memorial Centre, Intramural Grant, Grant/Award Number: None

DATA AVAILABILITY STATEMENT

We confirm to the journal policy for data availability. The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Data Availability Statement

We confirm to the journal policy for data availability. The data that support the findings of this study are available from the corresponding author upon reasonable request.

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