Clinical assessment of magnetic resonance imaging‑guided radiofrequency ablation for breast cancer

  • Authors:
    • Jian Li
    • Dan‑Dan Wang
    • Yu‑Nian Zhao
    • Jian‑Wei Zhou
    • Jin‑Hai Tang
  • View Affiliations

  • Published online on: August 2, 2019     https://doi.org/10.3892/mco.2019.1905
  • Pages: 411-415
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Abstract

The aim of the present study was to investigate the efficacy of magnetic resonance imaging (MRI)‑guided radiofrequency ablation (RFA) for breast cancer patients who cannot undergo traditional surgery. A total of 10 patients were treated by MRI‑guided RFA, of whom 6 had stage IV disease (lung metastasis n=3, bone metastasis n=1, liver metastasis n=1 and mediastinal metastasis n=1) and the remaining 4 patients, who refused surgery, had stage III disease accompanied by severe underlying conditions. The changes in feasibility, tumor volume, bleeding, local recurrence, metastasis and complications were evaluated after RFA. The patients were followed up at 1, 3, 6 and 12 months, and annually thereafter. A total of 14 RFA sessions were successfully performed (100%) in the 10 patients, among whom 7 patients underwent a single RFA session, 2 patients underwent two sessions, and 1 patient underwent three sessions. Compared with pre‑RFA, the volume of the tumors at 6 months after RFA was markedly decreased. There was no local tumor recurrence or metastasis detected during a mean follow‑up period of 19.5±3.46 months, and no major complications were reported. Therefore, RFA was found to be a minimally invasive and feasible treatment method in the present study, and MRI‑guided RFA may be a promising alternative option for breast cancer patients who are unable to tolerate surgery. However, more prospective studies on the applicability of RFA in breast cancer are required.

Introduction

Breast cancer is one of the leading cause of cancer-related deaths in women worldwide (1). Surgery is the mainstay of treatment for breast cancer; however, a large number of patients are unable to undergo surgery due to advanced cancer or severe underlying conditions, such as malignant hypertension, diabetes mellitus, poor heart and/or lung function. Therefore, new treatment strategies are urgently required for breast cancer patients with a high surgical risk. Over the past years, several such methods had been investigated, including high-intensity focused ultrasound, laser ablation, microwave ablation and radiofrequency ablation (RFA) (25).

RFA is an established procedure that has been widely used in various types of cancer, such as bone metastases, renal cell carcinoma, hepatocellular carcinoma (HCC) and breast cancer (4,68). RFA is a local, minimally invasive approach that is accompanied by fewer complications compared with other methods. For example, Lee et al (9) reported that RFA was associated with a better overall and progression-free survival compared with transarterial chemoembolization in single HCC. Chen et al (10), confirmed that computed tomography (CT)-guided RFA was feasible, effective and safe for inoperable pulmonary tumors. A meta-analysis of 15 studies demonstrated that RFA achieved a higher complete ablation rate and a low complication rate in breast cancer, proving that this method is effective and safe (11). However, whether patients diagnosed with advanced breast cancer or synchronous severe underlying conditions can benefit from RFA remains to be investigated.

In the present study, the efficacy of magnetic resonance imaging (MRI)-guided RFA was evaluated in patients with breast cancer at an advanced stage or with a high surgical risk.

Patients and methods

Patients

The study was conducted at the Department of Breast Surgery of Jiangsu Cancer Hospital and all eligible patients provided written informed consent prior to treatment. Between January 2015 and December 2015, 10 patients were diagnosed by coarse-needle puncture and were all confirmed as invasive breast cancer. All patients were assessed based on MRI, CT and related data. Patients with bone metastases were evaluated by emission CT (ECT). The inclusion criteria for RFA were as follows: i) Age >18 years; ii) diagnosis confirmed by pathology; iii) tumor size ≤3 cm; iv) tumor distance from the chest wall ≥1 cm; v) TNM stage IV; vi) TNM stage III with severe underlying disease; and vii) tumor refractory to various treatments and patient refusing to undergo surgery, chemotherapy and radiotherapy. The exclusion criteria included tumor size >3 cm, distance from the chest wall <1 cm, multifocal lesions and good outcome predicted with systemic chemotherapy or radiotherapy. Prior to the initiation of this study, all patients provided written informed consent and the study protocol was approved by the Ethics Committee of Jiangsu Cancer Hospital and Nanjing Medical University.

RFA procedures

Two professional radiologists performed the RFA procedures. All patients underwent routine blood tests, coagulation function and liver function assessment prior to RFA. Tumor stage was assessed by B-mode ultrasonography, CT and MRI. RFA was performed using MedSphere S500 (Medsphere, Carslbad, CA, USA) under MRI guidance (Philips Healthcare, Amsterdam, The Netherlands) and a 17-Ga insulated magnetic-free needle (BD Biosciences, Franklin Lakes, NJ, USA) with an ablation range of 2.5–3.0 cm.

Local anesthesia and disinfection were performed prior to RFA and the needle was inserted into the tumor. Then, MRI scanning at the cross-section, coronal and sagittal planes was performed to obtain three-dimensional stereoscopic images, which confirmed that the needlepoint was at least 0.5–1.0 cm inside the tumor. At the same time, the volume of tumor was calculated by MRI. Additionally, the power of RFA was gradually adjusted to 50 W and the temperature of the needle tip was maintained at 100°C over 5–10 min. During the process, 0.9% NaCl2 with 0–5°C was circulated into the system continuously to ensure uniform energy distribution. After ablation, the tumor size and blood flow were accessed by MRI. If there was residual tumor, an additional RFA session was immediately performed. After RFA, the patients were observed for 1 h and any complications were recorded.

Follow-up and outcome measurements

After RFA, all patients were followed up at 1, 3, 6 and 12 months, and annually thereafter: i) The size was assessed by physical examination (palpation); ii) the size, bleeding and apparent diffusion coefficient (ADC) value of the tumor were assessed by MRI; and iii) the size, bleeding and calcification of the tumor were assessed by breast X-ray. Complete remission (CR) was defined as complete disappearance of the tumor and no enhancement on MRI enhanced scan. Partial remission (PR) was defined as a decrease in the tumor volume of >50% and non-enhanced area of >50% on MRI. Stable disease (SD) was defined as a decrease in the tumor volume of <50% or an increase of <25%, and a non-enhanced area <50%. Progressive disease (PD) was defined as an increase in the volume of the tumor of >25%.

Ethics

The procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional or regional) and with the Helsinki Declaration of 1975, as revised in 2000 (https://www.wma.net/what-we-do/medical-ethics/declaration-of-helsinki/).

Statistical analysis

Statistical analysis was performed with SPSS 21.0 software (SPSS Inc., Chicago, IL, USA). The pre-/post-treatment volumes were calculated as V=πabc/6 (V, volume; a, largest diameter; and b and c, the two other perpendicular diameters). The data are presented as mean ± standard error of the mean. Chi-squared and Fisher's exact tests were used to assess the significance of each clinicopathological factor. Student's t-test was used to evaluate the differences in tumor volume, bleeding and ADC value. P<0.05 was considered to indicate statistically significant differences.

Results

Patient and clinicopathological characteristics

A total of 10 breast cancer patients who were unable to undergo conventional surgery presented to the Jiangsu Cancer Hospital between January and December 2015. The clinical information of the 10 patients is summarized in Table I. All the patients were women, with a median age of 56 years (range, 48–83 years). A total of 6 patients had stage IV disease (lung metastasis n=3, bone metastasis n=1, liver metastasis n=1 and mediastinal metastasis n=1) and the remaining 4 patients had stage III disease accompanied by severe underlying conditions.

Table I.

Clinical characteristics of breast cancers prior to treatment with RFA.

Table I.

Clinical characteristics of breast cancers prior to treatment with RFA.

Immunohistochemisty

Patient no.SexAge (years)PathologyERPRHER2Reason for RFALocationLargest diameter (cm)Volume (ml)TNM stage
1F73IDC+++Lung metastasisL1.5×1.2×3.02.83T2N1M1
2F73IDC++Lung metastasisR2.69×1.55×1.63.49T2N1M1
3F57IDC+Lung metastasisR2.5×2.0×1.43.66T2N1M1
4F54IDC+Bone metastasisL2.6×1.4×1.52.86T2N0M1
5F50IDC+Mediastinal metastasisL3.0×2.5×2.12.75T2N0M1
6F56IDC+++Liver metastasisL1.8×1.2×1.51.70T1N1M1
7F59IDC++Refused surgeryL2.4×1.7×3.06.41T2N1M0
8F81IDC++Refused surgeryL2.1×1.1×3.03.63T2N0M0
9F80IDC++Refused surgeryR2.1×1.3×1.82.57T2N1M0
10F48IDC+++Refused surgeryR1.8×1.2×1.51.70T1N1M0

[i] ER, estrogen receptor; PR, progesterone receptor; HER2, human epidermal growth factor receptor 2; IDC, invasive ductal carcinoma; RFA, radiofrequency ablation; TNM, tumor-node-metastasis; F, female; R, right; L, left.

Outcomes following RFA

A total of 14 RFA sessions were performed in 10 patients, among whom 7 patients underwent a single RFA session, 2 patients received two sessions, and 1 patient received three sessions. Successful placement of the RFA probe was achieved in all patients (100%). After RFA, all the tumors became necrotic, the blood supply disappeared and no enhancement was observed on MRI (Figs. 1 and 2).

Compared with pre-RFA, the volume of the tumors at 6 months post-RFA had markedly decreased (Table II). No local tumor recurrence or metastasis were detected during a mean follow-up of 19.5±3.46 months (range, 15–25 months).

Table II.

Tumor volume pre- and post-RFA.

Table II.

Tumor volume pre- and post-RFA.

Patient no.Pre-RFA (ml)1 month post-RFA (ml)6 months post-RFA (ml)Volume reduction ratio (%)
12.832.800.2292.2
23.493.010.2892.0
33.662.810.1197.0
42.862.000.00100.0
52.751.850.00100.0
61.702.200.00100.0
76.414.120.4593.0
83.633.500.2493.4
92.572.230.1395.0
101.702.440.00100.0
P-value 0.12 <0.01

[i] RFA, radiofrequency ablation. Bold print indicates statistical significance.

Complications

All processes were successfully completed, without any procedure-related or severe complications. The RFA-related complications included one case of pain in the breast and one of perspiration, which were resolved with conservative management.

Discussion

Although combined-modality therapy has decreased the mortality of breast cancer, a number of patients are unable to undergo surgery due to the high surgical risk associated with old age, advanced stage and severe underlying diseases, or refusal to receive surgery, leading to cancer progression (1). Therefore, different therapeutic strategies are urgently needed. With the advances in technological innovations, new minimally invasive therapeutic alternatives for various solid tumors have been developed, particularly RFA (10,12,13). A systematic review of the relevant literature demonstrated that RFA is a feasible, safe and successful approach to breast cancer treatment, and is associated with only minor complications (14,15).

The present study confirmed the efficacy of MRI-guided RFA in breast cancers with a higher surgical risk. The RFA procedure was safe and all patients tolerated it well, without major complications. In terms of efficacy, RFA reduced the size of the tumor and prevented bleeding. Thus, RFA appears to be a viable treatment option for patients with breast cancer who are not surgical candidates. In addition, it has also been demonstrated that RFA may be used with ultrasound and CT (16). A number of studies have confirmed MRI as the gold standard for assessing the response of breast cancer to RFA treatment (1719); those studies reported that RFA may be performed in early-stage breast tumors (size range, 0.5–2.0 cm); however, the present study indicated that MRI-guided RFA may be an alternative treatment option for breast cancer patients who are not considered candidates for surgery. In addition, accumulating evidence indicates that the most common complications of RFA include pain, skin burns, fever, bleeding and infection, without serious RFA-related complications (11,20). Apart from breast cancer, benign breast diseases may also be treated by RFA. Li et al observed that patients with breast fibroadenoma exhibited rapid recovery, less extensive injury and shorter hospitalization after RFA (21).

Moreover, Wang et al demonstrated that RFA combined with transcatheter arterial chemoembolization prolonged the progression-free survival, median survival time and survival rate of breast cancer patients with liver metastasis (22). In a 4T1 breast cancer animal model, Chiu et al demonstrated that RFA combined with glycated chitosan controlled tumor progression through inducing potent antitumor cytokine responses (23). According to those studies, it may be hypothesized that RFA combined with various other therapies may be applied as rescue treatment for advanced cancers preoperatively or postoperatively, although more evidence-based studies on breast cancer are required.

There were certain limitations to the present study, such as the small number of patients and the fact that it was conducted at a single center. Further multicenter studies with a larger patient sample population are necessary to confirm our results.

In summary, RFA appears to be feasible, effective and safe for breast cancer patients who have surgical contraindications or refuse surgery. Additionally, the value of MRI-guided RFA combined with surgery, chemotherapy, radiotherapy and other treatments warrants further investigation.

Acknowledgements

Not applicable.

Funding

The present study was supported by grants from the National Key Research and Development Program of China (no. 2016YFC0905900), the ‘333’ Talent Project of Jiangsu Province [no. 4(2016)], the National Key Clinical Specialist Construction Programs of China [no. 544 (2013)] and the Natural Science Foundation of Jiangsu Province (no. BK20151579).

Availability of data and materials

The datasets generated and analyzed during the present study are available from the corresponding author on reasonable request.

Authors' contributions

LJ, WD and ZY were responsible for RFA operation. TJ and ZJ designed the current study and performed statistical analysis. All authors read and approved the final version of this manuscript.

Ethics approval and consent to participate

All patients provided written informed consent prior to enrolment. The study protocol was approved by the Ethics Committee of Jiangsu Cancer Hospital and Nanjing Medical University. The procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional or regional) and with the Helsinki Declaration of 1975, as revised in 2000 (http://www.wma.net/e/policy/17-c_e.html).

Patient consent for publication

All patients approved the publication of the current study.

Competing interests

The authors declare that they have no competing interests.

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APA
Li, J., Wang, D., Zhao, Y., Zhou, J., & Tang, J. (2019). Clinical assessment of magnetic resonance imaging‑guided radiofrequency ablation for breast cancer. Molecular and Clinical Oncology, 11, 411-415. https://doi.org/10.3892/mco.2019.1905
MLA
Li, J., Wang, D., Zhao, Y., Zhou, J., Tang, J."Clinical assessment of magnetic resonance imaging‑guided radiofrequency ablation for breast cancer". Molecular and Clinical Oncology 11.4 (2019): 411-415.
Chicago
Li, J., Wang, D., Zhao, Y., Zhou, J., Tang, J."Clinical assessment of magnetic resonance imaging‑guided radiofrequency ablation for breast cancer". Molecular and Clinical Oncology 11, no. 4 (2019): 411-415. https://doi.org/10.3892/mco.2019.1905