Research ArticleClinical Studies
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Metastatic Adenoid Cystic Carcinoma at the Base of the Tongue and Duplicate Breast Cancer Diagnosed During Restaging

KATEŘINA LICKOVÁ, VÁCLAV MANDYS, RENATA SOUMAROVÁ, MARTIN MICHNA and MARTIN ŠTEFFL
In Vivo November 2024, 38 (6) 3125-3130; DOI: https://doi.org/10.21873/invivo.13798

Abstract

Background/Aim: Adenoid cystic carcinoma (AdCC) is a rare malignant tumor that primarily affects the salivary glands but can also occur in other organs. Low incidence and unpredictable clinical behavior make AdCC one of the most difficult head and neck tumors to treat. Case Report: We present the case of a 54-year-old woman with AdCC localized at the base of the tongue, following radical surgical and oncological therapy. Due to advances in palliative oncological treatment, there is a more than five-year survival period before the progression of metastatic disease. Considering the rare occurrence of this disease, a literature search was also conducted, and therapy options are discussed. Ensuring a sufficient extent of the surgical procedure is still a challenge, and most specialists agree that subsequent postoperative radiotherapy reduces the risk of local recurrence. The effective dose of radiotherapy to the area of the primary tumor and lymph nodes is not clearly defined. Conclusion: The distinct biological behavior of AdCC results in varying sensitivity to chemotherapy or radiotherapy compared to treatments commonly used for head and neck squamous cell carcinomas. Treatment recommendations for these rarer tumors are based mainly on case reports and small clinical trials. The acquired therapeutic experience can contribute to prolonging the survival period of patients and improving their prognosis and quality of life.

Key Words:

Adenoid cystic carcinoma (AdCC) is a rare malignant tumor arising from different areas where secretory glands located, e.g., the lungs, vulva, mammary gland and head and neck area. AdCC accounts for 1-2% of all head and neck cancer. AdCC occurs mainly in the salivary glands, where it accounts for up to 10-15% of all malignant neoplasms (1, 2). Approximately 60% of AdCC arise in the major salivary glands, and more than 1/3 in the minor salivary glands of the oral cavity and sinonasal tract (2). Primary AdCC arising from the minor salivary glands of the tongue is rare (3).

AdCC is usually characterized by slow indolent growth, and usually with signs of perineural invasion (4, 5). The most common sites of late distant metastases are the lungs, bones, liver and brain (2). Progression is usually slow over the course of several years, but when bone metastases are present, progression is usually significant (6). Liver metastases of AdCC are generally considered to be part of disseminated disease, whereas isolated liver metastases are very rare (7). The lymph node metastases are less common, but the lymph nodes in high-grade AdCC tend to be significantly more affected by the metastatic process (2). AdCC lymph node metastases are a very negative prognostic predictor (6, 7)

The treatment of the early stages of AdCC is based on surgery and very careful follow up aiming at preventing recurrence or the development of distant metastases (8, 9). Compared to other head and neck cancers, complete resection of the tumor is much more challenging, and positive surgical margins are no exception.

Surgical treatment may be followed by adjuvant radiotherapy, depending on the extent of the disease. The results of studies evaluating the efficacy of current chemotherapy remain unclear (10). Chemotherapy is used as part of palliative treatment for metastatic disease (7, 11). The significance of immunotherapy in AdCC has not yet been precisely determined (12). Low incidence and unpredictable clinical behavior make AdCC one of the most difficult head and neck tumors to treat. The mortality rate of patients with AdCC in the head and neck area is high, and the overall five-year survival in patients with AdCC of the tongue is reported to be approximately 50% (9, 13). New findings regarding the diagnosis, therapy, and biological behavior of these rare tumors can help to define and modify treatment strategies in clinical practice.

Case Report

In September 2018, a 54-year-old woman was referred by a general practitioner for long-lasting non-specific discomfort in the oropharyngeal area to the Department of Otorhinolaryngology of the 3rd Faculty of Medicine and University Hospital Královské Vinohrady (FNKV). The patient had previously been treated for arterial hypertension, whereas the family oncological history was negative. The patient underwent an otorhinolaryngological examination and a magnetic resonance (Figure 1, Figure 2) scan was performed with a finding of a suspected tumor process in the oropharynx.

Figure 1.
Figure 1.

Magnetic resonance (sagittal) shows a suspicious tumor process in the oropharynx.

Figure 2.
Figure 2.

Magnetic resonance (axial) shows a suspicious tumor process in the oropharynx.

In November 2018, a biopsy was performed and AdCC was confirmed. According to the recommendation of a multidisciplinary team, resection of the base of the tongue and neck nodes on the right side of group I-V were indicated and immediately performed. A tumor localized on the base of the tongue with dimensions 35×17×12 mm (depth of invasion 12 mm) was found in the supplied resection, which histologically corresponded to AdCC with predominant cribriform to tubular structures, with a focal metaplastic/transdifferentiated component of squamous cell carcinoma, overall grade 2, probably arising from a small salivary gland. In some locations, a more conspicuous perineural propagation was evident, but a clear lymphovascular invasion was not proven. Carcinoma structures extended into the margin of the resection and into the peripheral edge in one limited section. A total of 30 lymph nodes were harvested during neck dissection but no carcinoma metastases were found (0/30). According to the TNM classification, the tumor was evaluated as pT2 pN0 (0/30) pM0 (14).

Based on the risk factors and the extent of involvement, adjuvant radiotherapy of 66 Gy was indicated for the high-risk area of tumor base, 60 Gy for the medium-risk area considering the risk of microscopic spread, and selectively 54 Gy for the low-risk area, all in 33 fractions using the intensity modulated radiation therapy (IMRT), simultaneous integrated boost (SIB) tomotherapy technique from January 2, 2019 to February 18, 2019. The patient managed the therapy with adequate manifestations of toxicity-radiodermatitis grade (gr.) I, xerostomia gr. I and dysphagia gr. I even according to RTOG (The Radiation Therapy Oncology Group). The patient had no symptoms of recurrence during follow-up care until 2020.

In September 2020, a computed tomography (CT) (Figure 3) scan showed multiple pulmonary metastases with borderline suspicious lymph nodes in the mediastinum and pulmonary hilae. There were no signs of recurrence in the area of the primary tumor of the base of the tongue or of lymphadenopathy in the neck area.

Figure 3.
Figure 3.

Computed tomography shows multiple pulmonary metastases with borderline suspicious lymph nodes in the mediastinum and pulmonary hilae.

With regard to the clear metastatic lung infliction and the biological behavior of the AdCC, systemic oncological therapy with cisplatin (80-100 mg/m2) and 5-FU (800-1,000 mg/m2) every four weeks for a total of six cycles was indicated. Three months after the end of the therapy in April 2021, restaging CT of the lungs was performed, and the number and size of lung lesions were determined. During another restaging at the end of 2021, the progression of multiple metastatic lesions in the lung area was shown using CT. According to previous studies and because of PD-L1 positivity, a second line of palliative therapy with nivolumab 240 mg every two weeks was indicated. The patient tolerated the therapy very well, but after the 10th cycle, a follow-up CT scan in April 2022 confirmed the progression of metastatic lesions in the lung area according to the iRECIST criteria. Therefore, the current treatment was terminated and further examination, which was carried out in July 2022, showed recurrence in the metastatic lung and a newly visible metastatic lesion in the brain. A change in the structure of calcification in the left breast was also shown, which had been monitored since 2018 during screening examinations on mammograms, as a suspected duplicate tumor. Due to the suspicious finding in the brain, an MRI was performed (Figure 4) and metastasis was confirmed

Figure 4.
Figure 4.

Magnetic resonance imaging of metastases in the brain dorsoparietal on the left side.

The plan was to start further palliative therapy, but the situation was complicated by a moderate course of COVID-19 with lower respiratory tract involvement, and the patient was prescribed Lagevrio.

In October 2022, after recovery from COVID-19, palliative whole brain radiotherapy (WBRT) in the 10×3 Gy regimen, up to a total dose of 30 Gy. was initiated. After radiotherapy, considering performance status and the possibility of duplicate tumor in the breast area, a third line of palliative systemic therapy was indicated – paclitaxel (80 mg/m2), weekly. The patient’s condition surprisingly stabilized and even improved after completing the 6th cycle of chemotherapy.

For the possibility of a duplicate breast cancer, a detailed examination of resistance in the left breast with biopsy verification was indicated by the multidisciplinary team. A core biopsy from this lesion showed invasive breast no special type (NST) carcinoma, grade 1-2, with 70% estrogen receptor positivity (DCS Inovation System clone SP1 antibody, Thermo Fisher Scientific, Waltham, MA, USA), weak progesterone receptor positivity (Novocastra NCL-L-PGR-312 antibody). Detection of Her2/neu (Ventana Pathway Antiher2/neu (4B5) 1+ antibody ROCHE s.r.o., Prague, Czech Republic) was negative. The proliferative activity of tumor cells was 10% (Zetacorb Ki67 antibody, MIB1 clone, BARIA s.r.o., Prague, Czech Republic).

Due to the unexpected response to paclitaxel therapy, biopsy verification of the lung metastases was subsequently performed to rule out dissemination of the breast tumor. Adenoid cystic carcinoma with a typical morphological structure was found in a core cut biopsy sample from a lung lesion, which was immunohistochemically negative for GATA3, estrogen receptor and CK20. Only the detection of CK7 in the glandular tubular component of the tumor was positive. The microscopic finding and the result of immunohistological examination excluded metastasis of breast cancer.

In June 2023, a liver metastasis was detected on CT (Figure 5). Subsequently, the analysis using DNA and RNA next generation sequencing (NGS) for disease progression was completed, where probably pathogenic variants (class 4-5) were represented in more than 5% of the examined regions: variant c was found in the gene serine/threonine kinase 11 (STK11) with variant allele frequency (VAF) of 4%. In the Oncology Knowledge Base (OncoKB database), treatment for the G163D mutation in the STK11 gene is listed for Pembrolizumab and Bemcemtinib; treatment is recommended only for patients with non-small cell lung cancer (NSCLC).

Figure 5.
Figure 5.

Computed tomography shows newly established suspicion of liver metastasis.

In addition to the examined genes, probable pathogenic or pathogenic variants (class 4-5) were detected in the examined areas of the tumor, including those in the EP300 gene (NM_001429.4), but no relevant treatments have been approved by the Food and Drug Administration. The mutation K363N was found in the SMARCB1 gene. Tazemetostat is indicated for the treatment of patients with this mutation is. However, this treatment is recommended for patients with all unsolid tumors. Microsatellite instability (MSI) was not shown in any of the five investigated areas, and the tumor was evaluated as MSI (stable). The performed gene analyses did not bring any valid results for the possibility of choosing treatment.

The progression to the liver, the brain metastases (Figure 6, Figure 7) and the deterioration of the performance status (PS; 3 according to the WHO) of the patient became more obvious with manifestations of general fatigue and malaise. With regard to her overall unfavorable condition and exhausted treatment options for AdCC, no further oncological treatment was indicated. Therapy of duplicate early stage of breast cancer with hormone receptor positivity and disseminated AdCC would not lead to prolongation of survival or improvement of quality of life, so the patient is now under the care of a palliative team with the “best supportive care” recommendation.

Figure 6.
Figure 6.

Computed tomography shows progression with the liver metastases.

Figure 7.
Figure 7.

Magnetic resonance shows progression of the metastases in the brain dorsoparietal on the left side.

Discussion

The most common malignant neoplasm is squamous cell carcinoma for which treatment options and therapeutic procedures are very precisely defined in the head and neck area (15). Rarer malignant cancers, such as AdCC, can also occur in this area. Due to the extensive local progression of this carcinoma with infiltration of surrounding tissues and perineural spread, dissemination is not rare even after radical surgical treatment (16). The different biological behavior of AdCC is responsible for unequal sensitivity to chemotherapy or radiotherapy commonly used in head and neck squamous cell carcinomas. Treatment recommendations for these rarer tumors are based mainly on case reports or small clinical trials.

The primary option for radical treatment is surgery, as described in the introduction. Ensuring a sufficient extent of the surgical procedure is still a challenge, especially in relation to the possible perineural spread and positive surgical margins. Most specialists agree that subsequent postoperative radiotherapy reduces the risk of local recurrence, but its significance in prolonging survival remains unclear due to the lack of evidence (17, 18). Owing to the properties of AdCC, postoperative radiotherapy is used in most centers, but the effective dose per tumor base or draining lymph nodes has not yet been clearly defined (19, 20).

Data on doses per tumor bed with positive resection margins vary considerably between studies. The therapeutic range of the total dose is quite wide, from 46 Gy to 66 Gy, but the most favorable data for survival without signs of local recurrence were for a total dose higher than 60 Gy (21, 22).

There are also no clear recommendations for the extent of the irradiated volume, routinely the skull base is included in the irradiated volume of postoperative radiotherapy, especially in cases where perineural tumor propagation is detected. Another question concerns elective irradiation of the local cervical lymphatic regions. Although the risk of lymphovascular invasion is low, in some studies it has been recommended to irradiate the primary lymphatic watershed according to the extent and location of the disease (20, 23). We also followed these recommendations in adjuvant therapy. We applied a dose of more than 60 Gy to the tumor base and considering the localization of the primary tumor in the area of the base of the tongue; we also added the lymphatic watershed to the irradiated volume. Based on restaging examinations after adjuvant treatment, it is possible to evaluate the response to therapy and local control of the disease as very good because the disease was under control for almost 2 years without signs of recurrence and without signs of lymphadenopathy in the head and neck area.

Our case in many ways confirms the data from previous cases of AdCC, especially regarding late lung metastasis. Despite three lines of systemic therapy, the progression of metastases was very slow, but persistent. In some cases, reduced sensitivity to platinum-based chemotherapy was also confirmed, with local control less than six months (24).

Immunotherapy, which is commonly used in the second-line treatment of metastatic and recurrent squamous cell carcinomas of the head and neck, and which demonstrated a clinically significant response in patients who experienced early progression after platinum-based chemotherapy, did not prove effective in our case, as we found progression after the 10th cycle of treatment (25, 26). Interesting was the sensitivity to paclitaxel therapy, which reduced the rate of progression of the disease and even temporarily improved the condition. Given the generally poor response to the cisplatin-based cytotoxic chemotherapy commonly used in head and neck cancers, taxol therapy could also play a role in the treatment of AdCC. More research is needed to clarify the significance of adjuvant radiotherapy and systemic treatment of advanced AdCC diseases.

Conclusion

Our case shows the importance of presenting patients with rare head and neck tumors. As far as AdCC is concerned, it emphasizes the locally indolent nature, the risk of late metastasis and the importance of quality medical care. The acquired therapeutic experience can contribute to prolonging the survival period of other patients and improving their prognosis and quality of life.

Acknowledgements

This work was supported by the Charles University research program Cooperatio - Oncology and Haematology; Medical Diagnostics and Basic Medical Sciences.

Footnotes

  • Authors’ Contributions

    All Authors reviewed the results and approved the final version of the manuscript. Kateřina Licková: Conceptualization; Investigation; Project administration; Resources; Visualization; Writing – original draft. Václav Mandys: Oversight and leadership responsibility for the research activity planning and execution, including mentorship; Writing – review & editing. Renata Soumarová: Investigation; Visualization; Writing – review & editing; Conceptualization; Data curation. Martin Michna: Investigation; Visualization. Martin Šteffl Provision of study materials.

  • Conflicts of Interest

    The Authors report no conflicts of interest in relation to this work.

  • Received July 27, 2024.
  • Revision received September 4, 2024.
  • Accepted September 9, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Metastatic Adenoid Cystic Carcinoma at the Base of the Tongue and Duplicate Breast Cancer Diagnosed During Restaging
KATEŘINA LICKOVÁ, VÁCLAV MANDYS, RENATA SOUMAROVÁ, MARTIN MICHNA, MARTIN ŠTEFFL
In Vivo Nov 2024, 38 (6) 3125-3130; DOI: 10.21873/invivo.13798
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