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First published online October 26, 2006
British Journal of Radiology (2007) 80, 267-273
© 2007 British Institute of Radiology
doi: 10.1259/bjr/91383984
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Full paper

Ultrasound-guided percutaneous radiofrequency ablation in elderly breast cancer patients: preliminary institutional experience

P-Y Marcy, MD1, N Magné, MD, PhD2, P Castadot, MD2, C Bailet, MD1 and M Namer, MD3

1 Radiology Department, Centre Antoine Lacassagne, 06189 Nice, France, 2 Radiotherapy Department, Institut Jules Bordet, 1000 Bruxelles, Belgium, 3 Medical Oncology Department, Centre Antoine Lacassagne, 06189 Nice, France

Correspondence: Nicolas Magné, Institut Gustave-Roussy, Department of Radiotherapy, 39, rue Camille Desmoulins, 94805 Villejuif, France. E-mail: nicolas_magne{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Conclusion
 References
 
Breast cancer is a major source of morbidity and mortality in the elderly population and the number of patients will increase by 30% in future decades. Surgery and endocrine therapy could be considered as the standard treatment in elderly breast cancer patients, but anaesthesia for surgery requires a specific approach taking into account physiological and psychological alterations secondary to ageing. In cases with major alterations of performance status, percutaneous radiofrequency ablation (RFA) could be substituted for the surgical treatment. The aim of the current study is to evaluate the efficacy and feasibility of this technique. Five tumours in four consecutive patients (aged 79–82 years) contraindicated for surgery with symptomatic cT1-2N0M0, positive oestrogen receptor status, low grade were treated by percutaneous radiofrequency–lump ablation under local analgesia, using percutaneous ultrasound guidance. Thermal lesions were produced with RF power 30 W, at a frequency of 500 kHz. Ultrasound-guided percutaneous biopsy of the RF treated breast was performed during the follow-up. We report a successful RFA lump ablation experience in the treatment of four tumours (4/5). One local recurrence occurred within 4 months after RFA. The other biopsies taken during the follow up showed all fat necrosis within the oil cyst and no malignant cells. One abscess occurred at 9 months within the treated area. After a mean follow up of 29.4 months, all the patients are still alive without any other signs of recurrence or metastases. Ultrasound-guided percutaneous RFA is safe and feasible in the management of breast cancer in elderly patients. Nevertheless, further large comparative studies are needed in order to validate such a minimally invasive procedure in current practice.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Conclusion
 References
 
Breast cancer is a major source of morbidity and mortality in elderly women. Women aged over 70 years comprise approximately 30% of the breast cancer population and this proportion will progressively increase in future decades [1, 2]. The prevalence and incidence of breast cancer in older women may increase by 30% over the next decade if the expansion of the older population continues at the present rate [3]. Elderly breast cancer patients are sometimes treated by radical surgery, but most treatments performed in this particular group of patients are represented by breast conservative surgery without axillary dissection associated with an accelerated radiotherapy (± endocrine therapy; ± chemotherapy) [4]. There is a paucity of data to substantiate that such an approach is better than a more radical one in terms of survival. Elderly patients may receive less aggressive treatment because of perceived presence of comorbidity as well as paucity of trial data for this age group (over 70 years) [5]. Many patients over the age of 70 years receive radiotherapy as standard treatment. Surgery and endocrine therapy could be also considered as the standard treatment in elderly breast cancer patients, but anaesthesia for surgery requires a specific approach taking into account physiological and psychological alterations secondary to ageing [6]. In particular cases with major alterations of performance status, minimally invasive techniques such as laser photocoagulation [7–9], ultrasound surgery [10–13], cryotherapy [14–19], thermotherapy [20] and radiofrequency ablation (RFA) [21–24] and percutaneous primary radiotherapy [25] are now available for the treatment of primary breast cancer. The integration of imaging and thermal therapy can provide a minimally invasive or even non-invasive alternative to breast surgery for small tumours. Ongoing trials seek to show safety and efficacy for laser, radiofrequency, microwave, cryoablation and focused ultrasound surgery. Nevertheless, these therapies must prove their equivalent or even greater efficacy compared with surgical outcomes and must demonstrate total ablation of the dominant lesion with negative margins, while sparing normal tissue beyond the target tissue [26]. Thus, all those techniques have to be carefully evaluated in terms of efficacy and safety in usual practice. Percutaneous RFA could substitute for surgical treatment in those cases where classical anaesthesia could be life threatening. The aim of the present study is to evaluate the feasibility and the efficacy of the RFA lumpectomy in the case of a single tiny breast neoplastic nodule with a mid-term follow up in four elderly breast cancer patients.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Conclusion
 References
 
Patients
We planned a prospective pilot study on four consecutive breast cancer patients aged >70 years referred to our institution during the year 2001. In all cases, written informed consent was obtained prior to intervention. The full initial protocol was approved by the local ethics committee. Data for the pathological characteristics of tumours were extracted from clinical charts. The main items in this form were age, histological type (ductal, lobular, other), tumour size (cT according to the UICC TNM classification, 6th edition) and CA 15-3 level. Patients had to present positive hormonal receptors (HR) status, a low histological grade according to Scarff–Bloom–Richardson grading and a cT1-2N0M0. The patients had to request a minimally invasive treatment because they were afraid of surgery, and/or also had relative contraindications for complete sedation (myocardial infarction, residual angor, severe hypertension, diabetes mellitus). The initial neoplastic lesions must be imperatively located distant to the skin, to the nipple and pectoralis muscle in order to have a sufficient space to create a minimum spherical ablation (see "Radiofrequency ablation procedure" section). Four patients aged from 79 years to 82 years old presented an invasive breast malignant nodule clinically corresponding to those characteristics. One patient had synchronous bilateral breast adenocarcinoma (invasive ductal and lobular adenocarcinomas of the right and left breast, respectively). Patients' characteristics are given in Table 1Go. The diagnosis of invasive carcinoma was made by full core needle biopsy (14G) under ultrasound guidance in three patients, and by percutaneous fine needle aspiration in the patient presenting with bilateral carcinoma. Physical examination and imaging (conventional mammogram, ultrasound, bone scintigram, chest radiogram and liver ultrasound) revealed localized disease, without lymphadenopathy or visceral metastases. Two patients underwent breast MRI before and after percutaneous treatment. The CA 15-3 level was mildly elevated to 42 UI l–1 (Nl < 25 UI l–1) in one patient, normal in two and not performed for the last one.


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  		Table 1. Patients' characteristics

 
All patients were given hormone therapy (letrozole: 2.5 mg daily) during the 3 months before RFA, allowing a mean decrease in tumour size from 32 mm to 24 mm on high frequency ultrasound. Letrozole was maintained after RFA procedure.

Radiofrequency ablation procedures
Percutaneous radiofrequency–lumpectomy was performed under local analgesia (lidocaine, subcutaneous injection), using ultrasound guidance under sterile conditions in the interventional radiology suite. RFA was applied between a large neutral electrode, leading to a high electric field line density in the region of the needle tip, and the 1.5 mmx1.1 mm non-isolated needle tip ablation electrode. Thermal lesions were always produced with RF power 30 W, at a frequency of 500 kHz, during a 12 min application time as recommended by the manufacturer (Elektrotom 104HF; Thermo-Berchtold Medizinelektronik Gmbh, Tuttlingen, Germany). A controlled interstitial needle perfusion of isotonic sterile saline solution (0.9% NaCl) was applied using an infusion pump (Perfusor Secura FT; Braun, France). The current flows from the uninsulated perfused electrode implanted in the tumour to a grounding pad applied externally to the skin. A feedback system controlling RF power application and saline infusion of the needle maintains power delivery. The RFA probe was designed to create a minimum spherical ablation volume of 3 cm diameter. Thermocoagulation included the tumour plus at least a 5 mm margin. The RFA probe was typically positioned parallel to the overlying skin under ultrasound guidance, and the procedure was carried out during real-time ultrasound monitoring. Ablation zones were visualized as cone-shaped hyperechogenic areas around the needle tip, experiencing the temperature increase. Vital signs were monitored and if the patient reported significant discomfort, the ablation was temporarily halted. On completion of the procedure, the lines were retracted and the needle withdrawn. A small ice pack was placed on the wound for up to 24 h after the procedure for comfort. The patient was discharged home once stable and free of sedative effects.

Evaluation and analysis
Clinical examination and breast imaging (ultrasound, mammogram, MRI when possible) were performed at 24 h, 1 month, 3 months and every 3 months during the first year, and every 6 months during the second year (GoFigures 1 and 2Go). At 3 months, ultrasound-guided percutaneous biopsy of the RF treated breast was performed in all cases.


Figure 1
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  		Figure 1. (a) Dynamic MRI sequences of the right breast after intravenous bolus injection of gadolinium. Serial T1 weighted gradient echo sequences before and 1 min, 2 min, 3 min and 6 min after gadolinium-DTPA intravenous bolus injection. Subtraction of pre-contrast from early post-contrast images shows a single 16 mm early contrast nodular enhancement before RFA. Its location is distant to the overlying skin, to the nipple area and to the pectoralis muscle. (b) MRI (sequence T1) at 1 month. Note the 50 mmx35 mm well-defined hypointense area delineated by a tiny contrast enhancement at the periphery, which is supposed to correspond to reactive granulation tissue around the avascular treated area.

 

Figure 2
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  		Figure 2. Lateral mammograms before and 6 months after RFA. The typically malignant 22 mm opacity in the upper right breast is distant to the skin and the nipple before treatment; fat necrosis is shown after RFA.

 

   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Conclusion
 References
 
All of the RFA procedures were technically successful (5/5). The mean duration of the treatment in the four patients was 14 min (12 min, 12 min for each tumour for the patient with bilateral tumours, 14 min and 18 min). One patient had ablation times greater than 12 min owing to a brief interruption necessitated by patient discomfort. Nevertheless, all patients have tolerated the RFA procedure well under local analgesia.

Mean follow up was 29.4 months (range 24–36 months). Clinical examination disclosed a painless, firm 40 mmx50 mm treatment mass in the treated area of the breast within the first 3 months, in all four patients. This showed fat necrosis within the oil cyst and no malignant cells in three patients. One local recurrence occurred within 4 months after RFA and the patient refused percutaneous or surgical therapy as well as adjuvant radiotherapy (Figure 3Go). However, she accepted hormone therapy after which the nodule remained stable. Three patients subsequently underwent conventional radiation therapy of the breast within 3 months after RFA and hormonal therapy was maintained in all patients.


Figure 3
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  		Figure 3. (a) Local recurrence. Appearance of a tiny opacity within the margin of the fat necrosis on mammogram. (b) Corresponding ultrasound image showing a solid mural nodule at the border of the oil cyst. Cytological aspiration was positive for invasive carcinoma. Note the vicinity of the tumour to the skin.

 
No acute complication was observed. Nevertheless one abscess occurred as a late complication at 9 months within the treated area for which aspiration was immediately performed under local anaesthetic. The abscess grew the Morganella morgani germ. This patient also underwent partial breast resection after 1 month.

At the time of writing, all the patients are still alive without any other signs of recurrence or metastases. In one patient the CA 15-3 level has decreased from 42 UI l–1 to 35 UI l–1 and then to 31 UI l–1 (Nl <25 UI l–1). In the other patients, CA15-3 remained stable. Thus, of the four patients, two have remained well with letrozole, RFA and radiotherapy, one had local disease recurrence (that has remained stable for 36 months with letrozole), and one had a late abscess at 9 months that needed partial breast surgery.


   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Conclusion
 References
 
According to Vlastos et al, the distribution of disease by stage among elderly women (>70 years) is mainly Stage I–II disease in 92% of the cases. Comorbid conditions that may influence treatment planning are reported in up to 50% of the patients. The locoregional recurrence at 4 years median follow up is 5%, and occurs almost exclusively at the original tumoural bed. The distant metastases rate is 11% (mainly in the lung), and the 5 year and 10 year disease specific survival rates are 96% and 91%, respectively [27].

The challenge for interventional radiologists is to ablate the primary tumour without surgery using a minimally invasive percutaneous treatment in elderly patients who fear or have contraindications to surgery. Radioguided surgery, an alternative to traditional surgery, includes different approaches; with a goal to excise the primary tumour percutaneously (ABBI), cool it (cryotherapy), heat it (focused ultrasound, laser interstitial therapy or RFA) [25, 28–32] or irradiate it [25].

Böhm et al [28] demonstrated the in vitro feasibility of saline-enhanced RFA for the treatment of breast tumours. Interstitial perfusion is important to improve the electrical conditions for ablation by the spread of hot liquid. The irregular expansion of RF lesions may be due to the inhomogeneous tissue impedance resulting in electrical inhomogeneities and irregular heating or the presence of multiple ductal structures which may result in possible propagation of the hot emulsion into the surrounding tissue, a high infusion rate of interstitial saline solution. The authors concluded that percutaneous thermolysis is feasible with a better control of lesion localization with a low saline interstitial infusion rate [28]. Optimal NaCl concentration (38.5% saturated solution) of the interstitial saline solution may increase energy deposition, tissue heating and induced coagulation [29]. We think that peritumoural fatty breast tissue and the early stage of the tiny breast cancer in older patients are likely to reduce the problems of irregularity in thermolysis/RFA.

The first feasibility study of RFA in human breast tumours was reported in 1999 by Jeffrey et al who performed RFA in five women with locally advanced breast cancer (4–7 cm). Surgical excision of the treated area showed complete tumour ablation in four patients and a small area of viable cell lining a cyst in the fifth patient. The authors concluded that RFA may be most effective for the treatment of cancers smaller than 30 mm [30]. Size reduction of larger tumours may be obtained after hormonal therapy as in the present study.

Izzo et al reported a 96% complete necrosis rate in tumours less than 30 mm, under ultrasound control of T1 and T2 breast carcinomas [32]. One patient had a microscopic focus of viable tumour adjacent to the needle shaft site, which may be explained by electrical inhomogeneity and irregular heating during thermal ablation. Furthermore, we think that the radiopathological correlations are not optimal in invasive lobular carcinoma of the breast due to the particular anatomical tissue structure and may explain the local tumour recurrence in the present study despite its small size (less than 20 mm). Thus, is RFA a good choice in invasive lobular breast carcinoma?

According to the literature, potential complications induced by RFA may include occasional sepsis, haemorrhage, skin burns in a tumour immediately beneath the skin, residual firmness within the treatment region (clinical sign for fat necrosis) [33] and potential needle tract seeding [32–35]. One abscess developed late (9 months) after RFA, and thus was not thought to be directly related to the procedure. Nevertheless, Morganella morgani superinfection of the retroareolar fat necrosis area was probably due to an insidious retrograde colonization of these bacterias from the skin through the ductal canals. One has also to keep in mind potential complications such as skin burns, damage of the intercostal nerves, of the pericardium and other thoracic structures, fat necrosis, scarring, before RFA procedure.

Particular attention may be paid to the original tumour bed, and also along the needle tract: a 1.2–12.6% risk of seeding of neoplastic cells has been described in patients with RFA-treated hepatocellular carcinomas, along the needle pathway [34, 35]. The increasing size of the lesion on mammogram and nodular enhancing areas on MRI may suggest tumour recurrence at follow up [36]. MRI is very sensitive to tissue-water mobility and distribution and the temperature dependence of MR relaxation parameters such as T1 relaxation times and diffusion coefficients make it particularly suitable for the demonstration of thermal energy deposition in breast tissue (Figure 4Go). Potentially, the use of real-time MRI to monitor RFA in breast carcinomas, and the availability of open-access breast coils may facilitate complete tumour ablation with MR-compatible needles, in the future [37]. Moreover, MRI may depict any further recurrence of the tumour earlier than ultrasound/mammogram/clinical examination [36].


Figure 4
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  		Figure 4. Dynamic MRI of the treatment area at 3 months and 6 months, before and 1 min, 2 min, 3 min, 4 min and 6 min after intravenous gadolinium. Note the three distinct areas of the breast: the nipple area enhances early; the 50 mmx70 mm central fat necrosis does not enhance at all; the peripheral area (area 2) abnormally. 3 months later, an air–fluid level developed within the fat necrosis, the hypervascular margin was proved to be the granuloma located at the periphery of the pyogenic abscess.

 

   Conclusion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Conclusion
References
 
RFA may be a reasonable less invasive alternative to lumpectomy in elderly patients with selected early carcinoma of the breast with comorbid conditions, handicapped by mobility and/or transportation problems or who fear surgery. One could also recommend treatment of only ductal invasive carcinoma because these types of histological subtype have a well delimited tumour in the breast compared with lobular invasive carcinoma. Appropriate lesions must be located distant to the skin, to the nipple and pectoralis muscle with a sufficient margin of clear tissue. Large controlled studies are nevertheless required to validate the efficacy of this therapy in elderly patients with early stage malignant breast disease.

Received for publication March 23, 2006. Revision received August 21, 2006. Accepted for publication September 8, 2006.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Conclusion
 References
 

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