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Case ReportClinical Studies

Pembrolizumab and Radiotherapy for Platinum-refractory Recurrent Uterine Carcinosarcoma With an Abscopal Effect: A Case Report

MITSUTAKE YANO, SAKI ASO, MIHO SATO, YOKO AOYAGI, HARUNOBU MATSUMOTO and KAEI NASU
Anticancer Research July 2020, 40 (7) 4131-4135; DOI: https://doi.org/10.21873/anticanres.14412
MITSUTAKE YANO
1Department of Obstetrics and Gynecology, Nakatsu Municipal Hospital, Oita, Japan
2Department of Obstetrics and Gynecology, Faculty of Medicine, Oita University, Oita, Japan
3Department of Pathology, Saitama Medical University International Medical Center, Saitama, Japan
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  • For correspondence: yano1210@oita-u.ac.jp
SAKI ASO
1Department of Obstetrics and Gynecology, Nakatsu Municipal Hospital, Oita, Japan
2Department of Obstetrics and Gynecology, Faculty of Medicine, Oita University, Oita, Japan
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MIHO SATO
1Department of Obstetrics and Gynecology, Nakatsu Municipal Hospital, Oita, Japan
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YOKO AOYAGI
1Department of Obstetrics and Gynecology, Nakatsu Municipal Hospital, Oita, Japan
2Department of Obstetrics and Gynecology, Faculty of Medicine, Oita University, Oita, Japan
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HARUNOBU MATSUMOTO
1Department of Obstetrics and Gynecology, Nakatsu Municipal Hospital, Oita, Japan
2Department of Obstetrics and Gynecology, Faculty of Medicine, Oita University, Oita, Japan
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KAEI NASU
2Department of Obstetrics and Gynecology, Faculty of Medicine, Oita University, Oita, Japan
4Division of Obstetrics and Gynecology, Support System for Community Medicine, Faculty of Medicine, Oita University, Oita, Japan
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Abstract

Background: Immune responses due to radiotherapy and immune checkpoint inhibitors potentially have synergistic effects. Case Report: Here, we report a 65-year-old Japanese woman presenting with high-grade endometrial cancer. She was diagnosed with carcinosarcoma, stage IB. A month post-surgery, lung, and mediastinal lymph node metastasis/recurrence was detected. Progressive disease (with high microsatellite instability) with local recurrence and bone metastasis was detected after six chemotherapy cycles with paclitaxel and carboplatin. After combination therapy with pembrolizumab (2 mg/kg, tri-weekly, 10 cycles) and pelvic radiotherapy (30 Gy/10 fractions), enhanced computed tomography revealed a complete response. The patient survived for 14 months with the residual tumour post-relapse. This is the first case of a complete response of recurrent endometrial carcinosarcoma upon combinatorial pembrolizumab and radiotherapy. Conclusion: Combinatorial immune checkpoint inhibitors and local radiotherapy cause the abscopal effect and may be a promising treatment strategy for advanced or recurrent carcinosarcomas refractory to traditional chemotherapy.

  • Carcinosarcoma
  • endometrial neoplasms
  • microsatellite instability
  • pembrolizumab
  • radiotherapy
  • abscopal effect

Uterine carcinosarcomas, also known as malignant mixed Mullerian tumours, represent <5% of malignant uterine neoplasms. They are aggressive uterine cancers with poor survival rates, even at an early stage. The presence of heterologous elements signifies a poor prognosis even in patients with stage I uterine carcinosarcoma. Advanced or recurrent disease portends a severe prognosis, and its median progression-free survival/overall survival is 5.8-7.6 months/13.5-14.7 months, respectively (1, 2). Adjuvant chemotherapy comprising paclitaxel and ifosfamide (1)/paclitaxel and carboplatin (2) is administered after surgery; however, its effectiveness is limited, thus warranting the development of new therapies.

Tumours evade the immune system through distinct pathways including endogenous “immune checkpoints” that normally terminate immune responses after antigen activation (3). A recent study reported that solid tumours with DNA mismatch repair deficiency (4) and/or high microsatellite instability (MSI) (5) are highly responsive to pembrolizumab, thus prolonging patient survival. However, few studies have reported complete responses in MSI-high carcinosarcomas treated with only pembrolizumab.

The abscopal effect, initially reported by Mole in 1953 (6) upon administering local radiotherapy, is considered a systemic anti-tumour immune response, reflecting the regression of non-radiated metastatic lesions distant from the primary site of radiotherapy. Because immune checkpoint inhibitors can enhance the systemic anti-tumour response to radiotherapy, combinatorial radiotherapy and immunotherapy has received increasing attention (7). Herein, we report a case of uterine carcinosarcoma refractory to traditional chemotherapy, presenting a complete response to combinatorial immune checkpoint inhibitor and local radiotherapy.

Case Report

A 65-year-old Japanese woman, gravida 2, para 2, without any history of cancer, with pollakiuria and atypical genital bleeding, visited another clinic. An intrauterine mass was detected through transabdominal ultrasonography, and she was referred to our hospital for evaluation and treatment. She had a history of Meniere's disease. Her family history included a cancer of unspecified origin in her elder sister. Magnetic resonance imaging revealed the presence of a 58×50×40-mm3 mass in the uterine cavity (Figure 1A). No metastasis was detected on systemic computed tomography (CT). Serum levels of cancer antigen 125, cancer antigen 19-9, and cancer antigen 72-4 (tumour markers) were 201 U/ml, 2.8 U/ml, and 1.8 U/ml, respectively. Endometrial biopsy suggested high-grade endometrial carcinoma. She underwent an abdominal semi-radical hysterectomy, bilateral salpingo-oophorectomy, subtotal omentectomy, pelvic lymphadenectomy, and para-aortic lymphadenectomy. Macroscopically, the mass present in the lower segment of the uterine body had a polypoid appearance (Figure 1B). Histological analysis revealed that the tumour was a prominent undifferentiated carcinoma with necrosis (Figure 1C), endometrioid adenocarcinoma, squamous cell carcinoma, chondrosarcoma (Figure 1D), and osteosarcoma, having infiltrated >50% of the uterine myometrium. Furthermore, tumour nests contained peritumoural and tumour-infiltrating CD8+ lymphocytes at high density (Figure 1E, F). Lymphovascular invasion was detected. The tumour was diagnosed as a heterologous type uterine carcinosarcoma, stage IB, pT1b pN0 cM0 (International Federation of Gynecology and Obstetrics). Peritoneal cytological analysis revealed negative findings for malignancy. A week after surgery, no metastasis, recurrence, or residual tumour were detected through systemic CT. However, 1 month after surgery, systemic CT revealed lung and mediastinal lymph node metastasis/recurrence. The clinical course after recurrence is illustrated in Figure 2. The patient initially underwent systemic combined chemotherapy with paclitaxel (175 mg/m2) and carboplatin (areas under the plasma concentration-time curve of 6) (tri-weekly). After six chemotherapy cycles, enhanced CT revealed a progressive disease with local recurrence and bone metastasis. On immunohistochemical analysis, the tumour displayed PD-L1-positive foci (primary antibodies: 22C3 pharmDx, Dako North America, Carpinteria, CA, USA; and 28-8 pharmDx, Dako North America). Molecular analysis revealed high MSI in the tumour. Accordingly, treatment was switched to anti-PD-1 therapy with pembrolizumab (2 mg/kg, tri-weekly). After two cycles of pembrolizumab, she underwent resection surgery for a strangulated ileus. After three cycles of pembrolizumab, she received palliative radiotherapy (30 Gy/10 fractions) for genital bleeding from a vaginal tumour. After ten cycles of pembrolizumab, enhanced CT revealed a complete response. Lung and mediastinal lymph node metastases, local recurrence, and bone metastasis were difficult to identify. Two months after the complete response, brain metastases were detected. Since the detection of initial recurrence, the patient survived for 14 months after pembrolizumab therapy, with a residual tumour.

Figure 1.
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Figure 1.

Magnetic resonance imaging, macroscopic, and microscopic analysis of the endometrial carcinosarcoma. (A) T2-weighted image revealed a 58×50×40-mm mass in the uterine cavity (arrows). (B) The mass is a polypoid tumour in the endometrium (arrows). The tumour had (C) undifferentiated carcinoma with necrosis and (D) chondrosarcoma. (E, H&E; F, CD8) Tumour nests are accompanied by high peritumoral and tumour-infiltrating CD8-positive lymphocyte densities.

Figure 2.
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Figure 2.

The clinical course of the present case from recurrence. Circles show (A) lung metastasis, (B) lymph nodes metastasis, and (C) local recurrence. All lesions worsened after paclitaxel (PTX) + carboplatin (CBDCA) therapy, but disappeared after combination of pembrolizumab and local radiotherapy.

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Table I.

Summary of carcinosarcomas treated using immunotherapy (anti-PD-1/CTLA4 antibody).

Discussion

This was the first case of platinum-refractory recurrent uterine carcinosarcoma to present a complete response to combinatorial pembrolizumab and radiotherapy. Table I lists cases of carcinosarcoma treated with immunotherapy with anti-PD-1/PD-L1/cytotoxic T-lymphocyte antigen-4 antibody (8-13). Five of seven patients primarily presented tumours in the genital tract; the remaining two cases, in the lungs and liver. Two cases including the present case, presented a complete response and the other five cases presented a partial response to immunotherapy. High MSI due to DNA mismatch repair deficiency is a biomarker of a favourable response to pembrolizumab in solid tumours (4, 5). However, Table I shows that two cases presenting a complete response (CR) were MSI-high and MSI-stable, respectively, and CR occurred regardless of the MSI status. A feature of CR cases is the combination of pembrolizumab and local antitumor therapy. Herein, pembrolizumab was administered in combination with radiotherapy and in another case, with cryoablation therapy. Recent studies have reported synergistic anti-tumour effects (abscopal effect) of immune checkpoint inhibitors and radiotherapy (14) or cryoablation (15). The prominent antitumor effect observed herein may be associated with the abscopal effect. The abscopal effect is an immune-mediated anti-tumour effect of local radiotherapy/cryoablation, which can trigger the regression of metastatic tumours distant from the site of local radiotherapy (7). Immune cells including T cells are activated through the cytotoxic effects of radiotherapy and display a synergistic effect with immune checkpoint inhibitors. Currently, phase I-III clinical trials are underway to verify the combination of immune checkpoint inhibitors and radiotherapy in various cancers, which may be a promising therapeutic strategy (7).

The limitation of this study is that it reports a single case; hence, further studies are required to assess additional cases before drawing robust conclusions. However, the prognosis of advanced or recurrent endometrial carcinosarcomas refractory to traditional chemotherapy is extremely poor (1, 2). Therefore, we believe that the course of the present case provides essential information regarding carcinosarcoma and its clinical management.

In conclusion, this study describes the case of platinum-refractory recurrent endometrial carcinosarcoma successfully treated with the combination of pembrolizumab and radiotherapy. The immune reaction caused by local radiotherapy is expected to have a synergistic effect with immune checkpoint inhibitors. Combinatorial treatment with immune-checkpoint inhibitors and radiotherapy should be considered for all advanced or recurrent carcinosarcomas refractory to traditional chemotherapy.

Acknowledgements

The Authors thank Mr. Kouichi Kamada and Prof. Masanori Yasuda, Department of Pathology, Saitama Medical University International Medical Center, for their technical support. The Authors also thank Editage (www.editage.jp) for English language editing.

Footnotes

  • Authors' Contributions

    Conception/design: Mitsutake Yano; Provision of study material or patients: Mitsutake Yano; Collection and/or assembly of data: Saki Aso, Miho Sato; Data analysis and interpretation: Yoko Aoyagi, Harunobu Matsumoto, Kaei Nasu; Manuscript writing: Mitsutake Yano; Final approval of manuscript: Mitsutake Yano, Saki Aso, Miho Sato, Yoko Aoyagi, Harunobu Matsumoto, Kaei Nasu.

  • Conflicts of Interest

    The Authors have no financial conflicts of interest to declare regarding this study.

  • Funding

    This study was supported by Grants-in-Aid from the Ministry of Education, Science, Sports, and Culture of Japan (Research Project Numbers: 19K16778 to M. Yano).

  • Received May 21, 2020.
  • Revision received June 5, 2020.
  • Accepted June 6, 2020.
  • Copyright© 2020, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved

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Pembrolizumab and Radiotherapy for Platinum-refractory Recurrent Uterine Carcinosarcoma With an Abscopal Effect: A Case Report
MITSUTAKE YANO, SAKI ASO, MIHO SATO, YOKO AOYAGI, HARUNOBU MATSUMOTO, KAEI NASU
Anticancer Research Jul 2020, 40 (7) 4131-4135; DOI: 10.21873/anticanres.14412

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Pembrolizumab and Radiotherapy for Platinum-refractory Recurrent Uterine Carcinosarcoma With an Abscopal Effect: A Case Report
MITSUTAKE YANO, SAKI ASO, MIHO SATO, YOKO AOYAGI, HARUNOBU MATSUMOTO, KAEI NASU
Anticancer Research Jul 2020, 40 (7) 4131-4135; DOI: 10.21873/anticanres.14412
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Keywords

  • Carcinosarcoma
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