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. 2024 Jan 25;13(2):111–118. doi: 10.1007/s13691-023-00646-2

Remarkable remission of symptomatic dermatomyositis after curative breast cancer surgery

Makoto Fujino 1,5,✉, Masahiro Kawashima 1, Hajime Yoshifuji 2, Ran Nakashima 2, Yosuke Yamada 3, Yoshiaki Matsumoto 1, Nobuko Kawaguchi-Sakita 4, Yukiko Mori 4, Fengling Pu 1, Ayane Yamaguchi 1, Kosuke Kawaguchi 1, Masahiro Takada 1, Masakazu Toi 1
PMCID: PMC10957833  PMID: 38524641

Abstract

Dermatomyositis (DM) is an autoimmune disease that causes proximal muscle weakness in the extremities leading to severe immobility and dysphagia. Approximately 20% of patients with DM are positive for anti-TIF-1γ antibody and frequently accompanied by malignant tumors. Although DM remission after tumor resection has been reported, the indications for surgery in patients with severe DM are unknown. Herein, we report a case of a 79-year-old Japanese woman who presented with breast cancer and anti-TIF-1γ antibody-positive DM. She became bedridden shortly after DM onset. Although pulsed steroid therapy, intravenous immunoglobulin, tacrolimus, and endocrine therapy with fulvestrant did not improve her symptoms, tumor resection with axillary lymph node dissection resulted in complete remission of the DM after 8 months. Immunohistochemistry revealed high expression of TIF-1γ in cancer cells, both in the primary tumor and axillary lymph nodes. Since the serum levels of anti-TIF-1γ antibody decreased after the surgery, the existence of breast cancer with TIF-1γ expression may have contributed to the worsening of DM. The present case suggests that curative surgery should be considered as a treatment option even if the patient has severe symptoms, such as immobility and dysphagia. Careful discussions with patients and multidisciplinary collaboration are essential to make surgery feasible, particularly for those with severe symptomatic DM.

Keywords: Breast cancer, Dermatomyositis, Paraneoplastic syndrome, Anti-transcription intermediary factor 1-gamma autoantibodies

Introduction

Breast cancer is the most common cancer among Japanese women, which affects one in nine women throughout their lifetime. Dermatomyositis (DM) is an idiopathic inflammatory myopathy often accompanied by malignancies, including breast cancer. It has been reported that 15–30% of adult-onset DM coincides with malignancy [1]. Among the several types of DM, the presence of autoantibody to transcription intermediary factor 1γ (TIF-1γ) is strongly associated with cancer-related DM.

Here, we report the case of a 79-year-old woman with luminal-type breast cancer accompanied by severe muscle weakness due to anti-TIF-1γ antibody-positive DM. The patient was bedridden and had severe dysphagia that developed immediately after the onset of DM. Steroid, intravenous immunoglobulin, tacrolimus, and endocrine therapy with fulvestrant did not improve the patient’s symptoms. However, the patient’s symptoms improved dramatically after the curative breast surgery. As there are no specific guidelines regarding the treatment of patients with breast cancer who have severe DM, a multidisciplinary discussion is essential for the treatment of breast cancer with symptomatic severe DM.

Case report

A 79-year-old woman with no relevant medical history presented with a mass in her left breast. It had been gradually getting larger and showed skin invasion (Fig. 1A); however, she had not visited the hospital for approximately 1 year since her activities of daily living (ADL) had been generally fine. She noticed a rash on her upper right arm that had spread to the whole body within a few days. She underwent a skin biopsy at a primary hospital and was diagnosed with DM (Fig. 1B). At this time, serum creatine kinase (CK) was mildly elevated to 310 U/L. Although the skin rash improved slightly with the steroid ointment, dysphagia, and muscle weakness appeared and worsened rapidly within a few weeks. She was unable to swallow or walk due to severe muscle weakness. She was referred to our hospital and admitted urgently. Physical examination revealed scaly rashes on the face and back, which were called heliotrope rashes and shawl signs, respectively (Fig. 1C, D). Rashes were also observed on the head, fingers, and other parts of the body. Nail abnormalities were also observed in the fingers. Weakness is predominantly observed in the proximal limb muscles. The patient was bedridden, and continuous aspiration of saliva was required because of severe dysphagia. Serum CK was elevated to 1787 U/L, and serum anti-TIF-1γ antibody was positive (112 index). Serum anti-MDA5, Mi-2, Jo-1 and ARS autoantibody were negative. Breast ultrasonography (Fig. 2A, B) and positron emission tomography/computed tomography (PET/CT) (Fig. 2C, D) showed a 50 mm mass in the outer part of the left breast and swollen lymph nodes in the ipsilateral axilla, suggestive of metastasis. Core needle biopsy and aspiration cytology confirmed an invasive breast carcinoma of no special type with axillary lymph node metastasis. The primary tumor was positive for estrogen receptor (approximately 80%) and negative for progesterone receptor and HER2. The Ki-67 labeling index was 7.3%. Collectively, her tumor was diagnosed as left luminal-type breast cancer, cT4bN2M0, cStage IIIB (UICC 8th).

Fig. 1.

Fig. 1

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A The mass with skin discoloration was on the outer area of the left breast. B Skin biopsy from the erythema on the right forearm. Mild infiltration of inflammatory cells and vacuolization in the epidermal basal layer were observed. An eosinophilic necrotic keratinocyte was also observed in the epithelial layer. C A scaly rash on the face showed typical feature of Heliotrope rash. D A scaly rash on the back showed typical feature of Shawl sign

Fig. 2.

Fig. 2

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A Ultrasonography showed an irregular mass in the outer area of the left breast suspicious for breast cancer. B A left axillary lymph node is swollen in a round shape, suspicious of metastasis. C 18F-fluoro-deoxy-glucose (FDG) PET/CT scan showed a significant uptake of FDG in the left breast mass. D 18FDG PET/CT scan showed the left axillary lymph nodes

Steroid therapy (prednisolone, 1 mg/kg) and total parenteral nutrition were initiated immediately upon admission. Although serum CK levels quickly decreased after steroid administration, there was no sign of symptom improvement. From 20 days after the admission, intravenous immunoglobulin (IVIG) was administrated (0.4 g/kg/day, 5 days), and fulvestrant (500 mg intramuscular injection) was started as a treatment for breast cancer. Tacrolimus was initiated (target concentration, 5–10 ng/mL) 30 days after admission and IVIG was repeated 48 days after admission. However, the muscle weakness and dysphagia continued to worsen during the course of treatment. Fulvestrant did not produce significant tumor shrinkage (Fig. 3A, B). After multidisciplinary discussions, curative surgery for breast cancer was planned to improve DM symptoms. To minimize perioperative complications, prednisolone was reduced from 1 to 0.4 mg/kg/day over a short period of time, and intensive interventions by the nutrition support team were initiated. On 66 days after admission, a left breast total mastectomy and axillary lymph node dissection were performed. The final diagnosis was invasive breast carcinoma of no special type: ypT4b (45 mm with skin invasion), ypN2a (8/29), ypStage IIIB (UICC 8th). Immunohistochemistry showed positive nuclear staining for TIF-1γ in the breast cancer cells both in the primary site and lymph node metastasis (Fig. 4A, B), whereas negative or weakly positive in the normal epithelial cells of the mammary gland (Fig. 4C). TIF-1γ expression was also found in the immune cells, in the axillary lymph nodes without metastasis (Fig. 4D). These TIF-1γ positive immune cells were suggested to be macrophages based on the expression of CD68, CD163, PU.1 (Fig. 5A–D). Two weeks after the surgery, anastrozole was started as adjuvant endocrine therapy, and the prednisolone dose was kept at 0.3 mg/kg/day. Radiotherapy was not administered. Her dysphagia began to improve 1 month after surgery, and she was able to walk and eat by herself 5 months after surgery. Her ADL completely recovered 8 months after surgery, and she was doing well without signs of recurrence 2 years after surgery (Fig. 6).

Fig. 3.

Fig. 3

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After 2 months of preoperative treatment, the left breast mass slightly shrinked from 40 mm (A) to 37 mm (B) in diameter on contrast CT, and the treatment effect was stable disease

Fig. 4.

Fig. 4

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TIF-1γ expression is positive in the nucleus of breast cancer cells at primary tumor (A) and at ipsilateral axillary lymph nodes (B) (×20). Scale bar 100 μm. C TIF-1γ expression is weakly positive in some adjacent normal mammary duct epithelial cells (×40). Scale bar 50 μm. D TIF-1γ expression in the nucleus of resident immune cells in the axillary lymph nodes without metastasis (×40). Scale bar 50 μm. The corresponding HE stainings were attached on the right panel

Fig. 5.

Fig. 5

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Expression of CD68 (A), CD163 (B), PU.1 (C) in the TIF-1γ positive resident immune cells in the axillary lymph node without metastasis. The corresponding HE staining was attached (D)

Fig. 6.

Fig. 6

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Clinical course of the patient: serum anti-TIF-1γ antibody decreased slowly after the surgery and the patient ADL was recovered accordingly

Discussion

We experienced a case of severe symptomatic DM positive for anti-TIF-1γ antibody whose symptoms were dramatically improved after curative surgery for coincided breast cancer. DM can be classified according to the type of myositis-specific autoantibody (MSA) and exhibits slightly different clinical features according to the type of MSA. Anti-TIF-1γ antibody is found in 52% of tumor-associated DM [2] and are often accompanied by severe skin symptoms and dysphagia [3]. Among the patients with breast cancer and DM, higher levels of serum anti-TIF-1γ antibody is associated with younger age, higher tumor grade, larger tumor size, and negativity for estrogen receptor [2]. In addition, it is associated with increased risk of metastasis (HR, 1.54; 95% CI 0.93–2.54; p = 0.09), shorter distant metastasis free survival (p = 0.091) and shorter overall survival (HR, 1.6; 95% CI 0.9–2.8; p = 0.09) [4].

We searched the PubMed database using the terms ‘breast cancer’ and ‘dermatomyositis’ from January 1990 to December 2021 and found the reports of a total of 46 cases of breast cancer with DM [1–3, 5–39]. In 46 cases, including the present case, the median age was 55 (32–84) years. Proximal muscle weakness was observed in 31 patients (66%) and dysphagia in 17 patients (36%). Twenty-three patients (50%) had elevated serum CK levels (mean, 3,180 units). Serum CK levels after surgery have been described in only two cases and were reportedly normalized after 2–3 months. The stage of breast cancer is described in 36 patients: stage I, 6 cases (17%); stage II, 11 cases (31%); stage III, 15 cases (42%); and stage IV, 4 cases (11%). Similar to our case, 20 patients were diagnosed with breast cancer after being diagnosed with DM. In these patients, the average interval from DM diagnosis to breast cancer diagnosis was 39 weeks. In contrast, 18 patients were diagnosed with DM after being diagnosed with breast cancer. Five patients were simultaneously diagnosed at the same time. Intriguingly, breast cancer recurrence was observed after the recognition of DM flare-ups in four cases.

Improvement in DM-related symptoms after breast cancer treatment was reported in 22 patients. The mean times to improvement were 8.7 weeks. Two patients did not show any improvement, and the outcomes of 18 patients were not stated. Among the improved cases, 12 improved after surgery [1, 6, 10, 18, 30–32, 34, 39], with an average of 10.8 weeks until improvement. Improvement during neoadjuvant chemotherapy was observed in three cases [3, 26, 38], and two patients underwent surgery thereafter. Seven patients showed improvement during palliative chemotherapy [5, 6, 9, 16, 25, 35, 37], and it took an average of 5 weeks until improvement.

In this literature review, we could identify very small number of cases of anti-TIF-1γ antibody-positive DM, potentially because this autoantibody has been discovered recently (in 2008). Anti-TIF-1γ antibody was examined in 12 cases, eight of which were positive for the anti-TIF-1γ antibody [1–3, 14, 17, 19, 23, 28, 29, 38]. The median age of anti-TIF-1γ antibody-positive cases was 61 (42–79) years old. Four of eight positive cases exhibited dysphagia, whereas only one of four negative cases exhibited dysphagia. Although the sample size was small, dysphagia was reported more frequently in the cases of breast cancer with anti-TIF-1γ antibody-positive DM.

Based on our literature review, chemotherapy can improve DM symptoms more quickly than surgery. However, chemotherapy was not feasible in our patient because she was very old and bedridden, and continuous aspiration of saliva was required owing to severe dysphagia. It was also difficult to judge whether the patient was eligible for curative breast surgery where general anesthesia was required. She was at high risk of surgical site infection and respiratory complications because of her poor nutritional status, severe dysphagia, and treatment with high-dose steroids. In particular, aspiration pneumonitis and difficulty weaning patients from mechanical ventilation are concerns. Therefore, careful discussion and collaboration between surgeons, physicians, and other medical professionals, such as the nutrition support team, are essential to proceed with the surgery for this patient.

It is unclear why our patient recovered completely after the breast surgery. Serum anti-TIF-1γ antibody titers slightly decreased after the operation and higher expression of TIF-1γ was observed in tumor cells than in adjacent normal ductal cells. These findings suggest that the expression of TIF-1γ in cancer cells might boost the production of autoantibodies against TIF-1γ that is responsible for the development of the symptomatic DM. TIF-1γ expression was observed not only in the tumor cells but also in the immune cells which appeared to be macrophages in the lymph nodes.

It should be noted that symptoms related to DM could improve slowly and it often takes several months since the initiation of treatment for DM. Our patient showed complete recovery approximately 6–8 months after surgery, suggesting that the surgery led to the improvement of DM. However, we could not exclude the possibility that she could improve with medications, such as fulvestrant and steroids.

In conclusion, curative breast surgery should be considered as an effective option in cases of breast cancer-related severe symptomatic DM refractory to medication. In cases of poor general condition, due to severe muscle weakness and dysphagia, multidisciplinary collaboration and sufficient informed consent are essential to prevent unfavorable outcomes related to surgery.

Acknowledgements

The authors thank Dr. Ayako Kojima, Department of Dermatology of Uji Takeda Hospital, the Center for Anatomical, Pathological, and Forensic Medical Research, Kyoto University Graduate School of Medicine for preparing the microscope slides. Explorative staining was performed with the approval of the Ethics Committee of Kyoto University Hospital (Protocol Number; G424).

Data availability

All data related to this report are available from the corresponding author upon reasonable request.

Declarations

Conflict of interest

Masahiro Kawashima received lecture fees from Pfizer Japan Inc., Daiichi Sankyo, Guardant Health AMEA, Eisai Co., Ltd., and Chugai Pharmaceutical Co., Ltd.. Masahiro Kawashima received research fundings from Nippon Kayaku Co., Ltd., and Kyowa Kirin Co., Ltd.. Nobuko Kawaguchi-Sakita has an endowed chair at Fujitsu, Meiji Seika Pharma, Yakult, NTT, PRiME-R, CANNON Medical, HUG, NTT-DATA, and IHC. Masahiro Takada received lecture fees from Chugai Pharmaceutical Co., Ltd., Astra Zeneca K.K., and Daiichi Sankyo. Masahiro Takada received research fundings from Astra Zeneca K.K., Daiichi Sankyo, Eisai Co.,Ltd., KBCRN, JBCRG, ABCSG, Yakult Honsha Co., Ltd., MedBis co., Ltd., and IQVIA Japan. Masakazu Toi has a leadership position of JBCRG, KBCRN, OOTR, and JBCS. Masakazu Toi has an advisory role of Daiichi-Sankyo, Eli Lilly and companies, Bristol Myers Squibb, Athenex Oncology, Bertis Inc., Terumo Corporation, and Kansai Medical Net. Masakazu Toi received lecture fees from Chugai Pharmaceutical Co.,Ltd., Takeda Pharmaceuticals, Pfizer Japan Inc., Kyowa Kirin Co., Ltd., Taiho Pharmaceutical Co., Ltd., Eisai Co., Ltd., Daiichi-Sankyo, Astra Zeneca K.K., Eli Lilly and companies, MSD K.K., EXACT Sciences, Novartis Pharmaceuticals, Shimadzu Corporation, Yakult, Nippon Kayaku Co., Ltd., Devicor Medical Japan K.K., and Sysmex Corporation. Masakazu Toi received research funding from Chugai Pharmaceutical Co., Ltd., Takeda Pharmaceuticals, Pfizer Japan Inc., Taiho Pharmaceutical Co., Ltd., JBCRG, KBCRN, Eisai Co., Ltd., Eli Lilly and companies, Daiichi Sankyo, Astra Zeneca K.K., Astellas Pharma Inc., Shimadzu Corporation, Yakult Honsha Co., Ltd., Nippon Kayaku Co., Ltd., AFI Corporation, Luxonus Inc., Shionogi Pharma Co., Ltd., and GL Sciences Inc.. The other authors declare that they have no conflict of interest.

Ethics approval

Research Ethics Committee approval was waved due to the nature of case report.

Informed consent

Informed consent was obtained from the patient included in this study.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Data Availability Statement

All data related to this report are available from the corresponding author upon reasonable request.

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