Abstract
Background:
Nuclear protein in testis (NUT) cancers, also known as midline cancers, tends to occur in organs near the midline, such as the nasal sinuses and mediastinum. NUT carcinoma is very rare and has a poor prognosis.
Case description:
We report the case of a 44-year-old female patient with sinonasal NUT carcinoma who presented with a soft tissue mass in the left frontal sinus, ethmoid sinus, and left nasal cavity on computed tomography; the tumor was poorly demarcated from the left rectus medialis. After discussion with a multidisciplinary team with expertise on head and neck tumors, the patient was considered inoperable, and definitive concurrent chemoradiotherapy (CCRT) was recommended. The patient underwent CCRT followed by three cycles of consolidation chemotherapy with albumin-bound paclitaxel and nedaplatin. Subsequently, the patient underwent 16 cycles of consolidation therapy with the programmed death–1 (PD-1) inhibitor tislelizumab. The immune-related adverse events included grade 2 hypothyroidism. After CCRT, consolidation chemotherapy, and consolidation immunotherapy, the patient achieved a favorable outcome. The patient survived for 31 months, and there were no signs of recurrence or metastasis during follow-up.
Conclusion:
At present, there is no clear consensus on the consolidation treatment plan after CCRT for sinonasal NUT cancer. We used consolidation immunotherapy for the first time and achieved good efficacy, providing an innovative and promising treatment plan for refractory sinonasal NUT cancer.
1 Introduction
Nuclear protein in testis (NUT) carcinoma is extremely rare and has mostly been reported in case studies; the main primary tumor sites are the chest and head and neck (1, 2). The main molecular feature is a rearrangement of the testicular nucleoprotein gene (NUTM1). Although NUTM1 can fuse to numerous different partner genes, it most frequently forms a BRD4-NUTM1 fusion oncogene related to NUT carcinoma (2). The prognosis is very poor, with a median survival of less than 1 year (3). The treatment options for NUT cancer include surgery, radiation therapy, and chemotherapy. Surgery is critical for the treatment of NUT cancer, and surgery combined with postoperative chemoradiotherapy or radiotherapy is associated with improved survival (4). For patients with inoperable tumors or those who refuse surgery, radical concurrent chemoradiotherapy (CCRT) is an alternative. Recent advances in treatment options for head and neck NUT cancer include induction chemotherapy, proton radiotherapy, and immunotherapy. The SINTART 1 study showed that patients with tumor shrinkage greater than or equal to 80% after induction chemotherapy for surgically resectable sinonasal tumors were given the option of radiotherapy and exemption from surgical treatment (5). The SINTART 2 study showed that the addition of induction chemotherapy to treatment regiments for inoperable sinonasal tumors did not significantly improve survival (6). The above two phase II studies of induction chemotherapy did not include NUT cancers, and only one retrospective study of NUT cancers has analyzed the value of induction chemotherapy. Ramesh et al. (7) conducted a retrospective analysis of 12 patients with sinonasal NUT cancer and concluded that induction chemotherapy may be beneficial to patients. Patients with recurrent sinonasal NUT may be considered for proton radiotherapy. Muramatsu et al. (8) reported a case of sinonasal NUT carcinoma with local recurrence followed by reirradiation using proton radiotherapy, which led to complete response. In recent years, the rapid development of immunotherapy has led to the development of new options and useful additions to treatments for NUT cancer, which is often refractory. Currently, treatment with PD-1 and programmed death–ligand 1 (PD-L1) inhibitors has been reported for a small number of patients with lung, thyroid, and parotid NUT cancer (9, 10) but has not yet been reported for sinonasal NUT cancer. Moreover, there is no standard for consolidation regimens after CCRT. This study aimed to explore new treatment options for NUT cancer and strategies for consolidation immunotherapy after CCRT: we report the treatment of one patient with sinonasal NUT cancer with immunotherapy with PD-1 inhibitors after CCRT.
2 Case presentation
The patient was a 44-year-old female from Shandong, China. She was first admitted to our hospital on 17 June 2021, with the complaint of left eye pain and headache for 3 months. She had undergone surgery for congenital heart disease 30 years prior. She was admitted to the hospital and underwent relevant examinations. Nasal endoscopy revealed a mass in the left middle nasal meatus adjacent to the left middle nasal turbinate (Figure 1). Biopsy pathology revealed that the tumor cells were blue, rounded, heterogeneous cells, some of which were naked nucleated cells with minimal cytoplasm (Figures 2A, B). Immunohistochemical (IHC) staining revealed tumor cells that were positive for NUT expression (Figure 2C). The Ki-67 mitotic index was nearly 70%. Epstein-Barr virus (EBV)-encoded RNA (EBER) in situ hybridization was negative. Based on NUT IHC, a diagnosis of NUT cancer was established. Further testing revealed positive PD-L1 expression in both tumor cells and immune cells (Figure 2D). The percentages of tumor cells and immune cells with PD-L1 positivity were 65% and 1%, respectively. Enhanced computed tomography (CT) of the sinuses revealed that most of the mass was located in the left ethmoid sinus, with the mass invading the frontal sinus upward, invading the medial orbital wall and the rectus medialis to the left, with a discontinuity of bone in the medial orbital wall on the left side of the orbital wall, invading the intracranial area upward, and breaching the wall of the floor of the sieve sinus downward into the middle nasal passages (Figures 3A–C). 18F-fluorodeoxyglucose (18F-FDG) PET/CT demonstrated hypermetabolic activity with increased fluorodeoxyglucose uptake in the ethmoid sinus mass (maximum standardized uptake value, SUVmax 27.7) (Figure 3D). Regional lymph node involvement and metastatic disease were also excluded. Considering the results of nasal endoscopy, paranasal sinus CT, and PET/CT, the final diagnosis was sinonasal NUT carcinoma (cT4bN0M0, stage IVA AJCC-8 version). After discussion with our multidisciplinary team (MDT) of experts on head and neck tumors, including the Department of Radiology, Pathology, Otolaryngology, Radiation Oncology and Medical Oncology, we concluded that the tumor was inoperable and recommended definitive CCRT. The patient agreed with the treatment plan derived from the MDT discussion and underwent definitive CCRT in our department. The gross tumor volume (GTV) contained macroscopic primary tumor detectable on CT imaging. The clinical target volume (CTV) was defined as the GTV plus a 5- to 10-mm margin to encompass the sites of microscopic extension including bilateral parapharyngeal space, bilateral retropharyngeal lymph node drainage area, left II–IV lymph drainage area, right partial II area, left cavernous sinus, bilateral sieve sinus and pterygoid sinus, frontal sinus, left maxillary sinus, nasopharyngeal, oropharyngeal, bilateral intrinsic nasal cavities, cranial base, bilateral pterygoid plate, pterygoid, medial pterygoid muscle, and pterygopalatine fossa. A planning target volume (PTV) was generated by incorporating a three-dimensional margin of 3 mm to the target volume in order to account for the uncertainties associated with treatment setup and internal organ mobility. The prescribed doses were 70 Gy and 60.06 Gy in 33 fractions, for the PTVs derived from GTV and CTV, respectively. Volume-modulated arc therapy technology was used to administer radiotherapy. During radiotherapy, the patient received three cycles of synchronized cisplatin chemotherapy (50 mg/m2 days 1–2 q3w) and sodium glycididazole (1.25 g days 1, 3, and 5 qw). According to the Response Evaluation Criteria in Solid Tumors, the efficacy of chemoradiotherapy (1 month after CCRT) was evaluated as a partial response (PR). Afterward, the patient received three cycles of consolidation chemotherapy with albumin-bound paclitaxel (260 mg/m2 day 1 q3w) and nedaplatin (80 mg/m2 day 1 q3w). The efficacy of three cycles of consolidation chemotherapy was evaluated as PR (Figure 3E). Considering that NUT cancer is a highly malignant tumor with a poor prognosis, subsequent consolidation immunotherapy was agreed upon after thorough communication with the patient. Sixteen cycles of consolidation therapy with intermittent tislelizumab (200 mg day 1) were started on 7 January 2022, and the last immunotherapy treatment was given on 6 December 2023. Details of the timing of the use of tislelizumab are given in the Supplementary File. After 16 rounds of immunotherapy, the ethmoid sinus lesions achieved a state of sustained remission, and the efficacy assessment revealed a PR (Figure 3F). Adverse effects throughout treatment are tolerable. Acute toxicity during radiotherapy is mainly characterized by localized radiodermatitis of the facial skin. According to the Radiation Therapy Oncology Group’s acute radiation morbidity scoring criteria for skin, acute radiation dermatitis was grade 1. There was no late toxicity after radiotherapy, and, to date, the patient has not experienced vision loss. The immune-related adverse events included grade 2 hypothyroidism. The recent workup on 6 December 2023 demonstrated no local recurrence or distant metastasis. The entire treatment timeline of the patient is shown in Figure 4.
Figure 1
Figure 2
Figure 3
Figure 4
3 Discussion
Sinonasal NUT carcinoma is very rare. There is a lack of large-scale epidemiologic studies and only a few retrospective studies with small sample sizes. A review of the literature by Lee et al. revealed that 4 of the 362 cases of poorly differentiated or undifferentiated carcinomas of the head and neck were sinonasal NUT carcinomas (11). A single-center study from China revealed that 3 of the 145 cases of sinonasal malignancies were NUT carcinomas (12). NUT has a very unfavorable prognosis. The median survival time for patients with primary NUT cancer of the chest is only 4.4 months (13). Compared to that for primary tumors in the lungs, the median survival time for primary NUT cancers of the head and neck is slightly greater, at only 9.7 months (13). In head and neck NUT cancers, survival may also vary depending on the location of the primary focus. A recent single-center study of 12 patients with sinonasal NUT carcinoma revealed median OS and median disease-specific survival times of up to 14.6 months (7).
Pathologic diagnosis of NUT cancer includes IHC and genetic testing, and genetic testing methods include fluorescence in situ hybridization (FISH), next-generation sequencing (NGS), and reverse transcription–polymerase chain reaction (RT-PCR) (14). Diffuse (>50%) positive NUT expression on IHC is sufficient for diagnosing NUT cancer (15). The diagnosis of NUTMI molecular rearrangements by FISH and NGS is not necessary, but the above two tests are helpful in determining the prognosis of NUT cancer patients (13). In this case, the patient was diffusely positive for NUT expression according to IHC, and the diagnosis was confirmed on this basis.
We reviewed the literature on sinonasal NUT cancer (7, 8, 12, 16–30) (Table 1). Treatment decisions were made on the basis of the above literature by first assessing the tumor stage. The treatments for locally advanced disease include surgery combined with postoperative adjuvant radiotherapy, definitive chemoradiotherapy, induction chemotherapy combined with surgery, and induction chemotherapy combined with radiotherapy. The treatments for metastatic disease include chemotherapy combined with immunotherapy and debulking surgery and chemotherapy combined with local palliative radiotherapy. Bromodomain and extra-terminal domain inhibitors may be an option after progression on first-line therapy for metastatic NUT cancer. In this case, tumor was considered late stage and considered to be unsuitable for surgical treatment by the MDT; ultimately, CCRT was selected as the treatment strategy. After CCRT, we first performed consolidation chemotherapy include albumin-bound paclitaxel and nedaplatin. There are few previous studies on consolidation chemotherapy after CCRT for sinonasal cancer. The consolidation chemotherapy regimen can refer to the induction chemotherapy regimen. The most commonly used induction chemotherapy regimens for sinonasal cancer are docetaxel and platinum (TP) and docetaxel, cisplatin, and fluorouracil (TPF) (31). TP includes paclitaxel and cisplatin, and TPF includes paclitaxel, cisplatin, and fluorouracil. These two consolidation chemotherapy regimens also provide a reference for consolidation chemotherapy for nasal sinus NUT cancer. At the end of CCRT and consolidation chemotherapy, the patient received consolidation immunotherapy based on three considerations. First, recent evidence has confirmed that consolidation therapy with immune checkpoint inhibitors (ICIs) can improve the survival of patients with lung and esophageal cancer after CCRT (32–34). In rare tumors, such as pulmonary sarcomatoid carcinoma (PSC) and pulmonary pleomorphic carcinoma (PPC), there are also case reports of encouraging results with consolidation immunotherapy after CCRT (35, 36). Although there is currently no evidence of survival benefits from ICI consolidation therapy after CCRT in patients with head and neck tumors, these findings in patients with lung and esophageal cancer can guide studies on head and neck tumors. A summary of clinical trials or case reports of consolidation immunotherapy after radiotherapy for malignant tumors is listed in Table 2 (32, 35–42). These clinical trials and case reports provide some reference for the selection of future consolidation ICI regimens after chemoradiotherapy for sinonasal NUT cancer patients. Second, although the patient’s treatment efficacy after radiotherapy was evaluated as PR, NUT cancer has a poor prognosis and is prone to recurrence and metastasis, and good recent treatment efficacy may not necessarily indicate a good long-term prognosis. Thus, maintenance therapy may be needed after radical treatment is completed. Maintenance therapy requires the selection of an agent that is both highly effective and less toxic, and PD-1 inhibitor immunotherapy may be an option. Third, the case in this study had high PD-L1 expression in tumor cells. High-dose anti–PD-1/anti–PD-L1 therapy is generally believed to indicate a greater response rate and clinical benefit when PD-L1 is expressed (43). According to a recent report from the NUT symposium, patients with PD-L1 positivity or a high tumor mutation load can receive ICIs in combination with chemotherapy (15). Additionally, there have been recent case reports of the combined use of immunotherapy in head and neck NUT cancers. One patient had thyroid NUT cancer combined with carelizumab immunotherapy in addition to postoperative chemotherapy (9). Another case involved parotid NUT cancer, which was treated with targeted agents combined with sintilimab immunotherapy after multiple postoperative metastases were detected (10).
Table 1
| Authors | Year | Number of patients | Location | Treatment | Outcome |
|---|---|---|---|---|---|
| Ramesh et al. (7) | 2024 | 12 | Nasal cavity maxillary sinus ethmoid sphenoid | Surgery ± induction chemotherapy; chemoradiotherapy ± induction chemotherapy | 14.6 months (median OS) |
| Caner et al. (16) | 2024 | 1 | Nasal cavity | Induction chemotherapy combined with immunotherapy + surgery + radiotherapy | 5.4 months (OS) |
| Qayum et al. (17) | 2024 | 1 | Maxillary sinus | Endoscopic sinus surgery+ maxillectomy | NM |
| Arai et al. (18) | 2024 | 1 | Maxillary sinus | Induction cheomotherapy + chemoradiotherapy (initial treatment); immunotherapy + targeted therapy and chemotherapy (after progression) | 11 months (OS) |
| Wang et al. (12) | 2023 | 3 | Nasal cavity maxillary sinus ethmoid | Surgery + radiotherapy | One patient 13 months (OS); two survived 12 and 15 months |
| Wartenberg et al. (19) | 2023 | 1 | Maxillary sinus | Surgery + radiotherapy | NM |
| da Costa et al. (20) | 2023 | 1 | Nasal cavity | Chemotherapy | NM |
| Zheng et al. (21) | 2023 | 1 | Maxillary sinus | Chemoradiotherapy + chemotherapy | NM |
| Wei et al. (22) | 2022 | 1 | Nasal sinus; frontal sinus | Surgery + radiotherapy | NM |
| Muramatsu et al. (8) | 2022 | 1 | Ethmoid | Chemoradiotherapy | survived 26 months |
| Patel et al. (23) | 2021 | 1 | Sphenoid | Ehemotherapy + radiotherapy (initial treatment); targeted therapy (after progression) | survived 21 months |
| Vakani et al. (24) | 2020 | 1 | Sphenoid | NM | NM |
| Oliveira et al. (25) | 2019 | 1 | Maxillary sinus | Induction cheomotherapy + chemoradiotherapy; chemotherapy (after progression) | NM |
| Arimizu et al. (26) | 2018 | 1 | Nasal cavity | Chemotherapy + chemoradiotherapy + surgery; chemotherapy + targeted therapy (after progression) | 9 months (OS) |
| Edgar et al. (27) | 2017 | 1 | Nasal cavity | Surgery + radiotherapy and chemotherapy | 3 months (OS) |
| Yang et al. (28) | 2015 | 1 | Nasal cavity | Surgery + radiotherapy and chemotherapy | Survived 10 months |
| Suzuki et al. (29) | 2014 | 1 | Nasal cavity | Chemoradiotherapy | Survived 12 months |
| Hsieh et al. (30) | 2011 | 1 | Nasal cavity | Chemoradiotherapy | NM |
Summary of previous studies reporting sinonasal NUT cancer.
NM, not mentioned.
Table 2
| Trial/NCT number/authors | ICI | Target | Dose | Frequency | Duration (time/cycles) | Cancer type |
|---|---|---|---|---|---|---|
| RATIONALE 311 (37) | Tislelizumab | PD-1 | 200 mg | q3w | 24 months | ESCC |
| Geng et al. (our case) | Irregular | 23 months | Sinonasal NUT cancer | |||
| NCT03671265 (38) | Camrelizumab | PD-1 | 200 mg | q2w | 32 weeks (from the beginning of radiotherapy) | ESCC |
| InTRist (39) | Toripalimab | PD-1 | 240 mg | q3w | 12 months or until progression | NSCLC |
| KEYNOTE-412 (40) | Pembrolizumab | PD-1 | 200 mg | q3w | 14 cycles | HNSCC |
| PACIFIC (32) | Durvalumab | PD-L1 | 10 mg/kg | q2w | 12 months or until progression | NSCLC |
| ADRIATIC (41) | 1,500 mg | q4w | 24 months or until PD or intolerable toxicity | SCLC | ||
| Wang et al. (36) | 620 mg | q2w | 12 months | PSC | ||
| Yorozuya et al. (35) | NM | NM | 12 months | PPC | ||
| JAVELIN Head and Neck 100 (42) | Avelumab | PD-L1 | 10 mg/kg | q2w | 12 months | HNSCC |
| NCT03377400 (34) | Durvalumab | PD-L1 | 1,500 mg | q4w | 24 months | ESCC |
| Tremelimumab | CTLA4 | 75 mg |
Summary of clinical trials or case reports of consolidation ICI after chemoradiotherapy in patients with different cancer.
ICI, immune checkpoint inhibitor; NCT, National Clinical Trial; PD-1, programmed cell death–1; PD-L1, programmed cell death–ligand 1; NM, not mentioned; q3w, every 3 weeks; q2w, every 2 weeks; q4w, every 4 weeks; CTLA4, cytotoxic T-lymphocyte antigen–4; ESCC, esophageal squamous cell carcinoma; NSCLC, non–small-cell lung cancer; SCLC, small cell lung cancer; HNSCC, head and neck squamous cell carcinoma; PSC, pulmonary sarcomatoid carcinoma; PPC, pulmonary pleomorphic carcinoma.
4 Conclusions
NUT carcinoma of the nasal cavity and sinuses is very rare, and only 50 cases have been reported in the literature. Surgery is the first choice for the treatment of NUT carcinoma, and CCRT can be chosen for patients who cannot be treated surgically. Compared with surgery, radiotherapy has the advantage of preserving organ function, thus improving the quality of life of patients. There is no consensus yet on consolidation treatment after CCRT. In this case, we studied a case of ethmoid NUT cancer that was treated with consolidation PD-1 inhibitor therapy after CCRT, which yielded a good therapeutic response. More case studies are needed in the future to validate the efficacy of consolidation immunotherapy after CCRT and to study the underlying mechanisms involved.
Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.
Ethics statement
The studies involving humans were approved by Ethics Committee of Weifang People’s Hospital. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study. Written informed consent was obtained from the individual(s) for the publication of any potentially identifiable images or data included in this article.
Author contributions
XG: Data curation, Writing – original draft, Writing – review & editing. XC: Data curation, Writing – review & editing. XW: Data curation, Writing – review & editing. SL: Writing – review & editing. GH: Data curation, Writing – review & editing. ZS: Data curation, Writing – review & editing. FH: Supervision, Writing – review & editing. JL: Conceptualization, Data curation, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the Medical and Health Science and Technology Development Program Project of Shandong Province (Grant No.202109030776).
Acknowledgments
We thank the patient for her trust in us, her cooperation with the treatment, and her informed consent for the publication of this case report. We would also like to thank all the doctors and nurses who were responsible for this patient’s treatment.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fonc.2024.1368187/full#supplementary-material
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Summary
Keywords
NUT, sinonasal, concurrent chemoradiotherapy, immunotherapy, PD-1 inhibitor
Citation
Geng X, Chang X, Wang X, Li S, Han G, Song Z, Hao F and Li J (2024) Consolidation immunotherapy following concurrent chemoradiotherapy in a patient with sinonasal NUT carcinoma: a case report. Front. Oncol. 14:1368187. doi: 10.3389/fonc.2024.1368187
Received
10 January 2024
Accepted
21 October 2024
Published
06 December 2024
Volume
14 - 2024
Edited by
Timothy James Kinsella, Brown University, United States
Reviewed by
Barbara Vischioni, National Center of Oncological Hadrontherapy, Italy
Xinmao Song, Fudan University, China
Updates
Copyright
© 2024 Geng, Chang, Wang, Li, Han, Song, Hao and Li.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Jianwen Li, Ljwwf112@163.com
Disclaimer
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