Minimally invasive ablative techniques in the treatment of breast cancer: a systematic review and meta-analysis

Figures & data

Figure 1. PRISMA 2009 flow diagram.

Table

(b)	Adequate sequence generation	Power analysis	Concealed allocation	Blinding	Incomplete data addresses	Free of other bias	Free selective reporting
HIFU	U	0/2	U	0/2	0/2	2/0	2/0
Microwave ablation	U	0/2	U	0/2	1/1	2/0	2/0

U: unspecified. Study quality was assessed according to the “Risk Bias Tool” in the Cochrane Handbook.

Table 1. Study characteristics and outcomes for (a) radio-frequency, (b) laser, (c) cryo, (d) high intensity focussed ultrasound and (e) microwave ablation.Table 1(a). Study characteristics and outcomes for radiofrequency ablation (RFA).

Study	N	Size lesion (cm)*	Age (years)*	Electrode^+	CA	Resection*	Complications	Treatment time (min)*
Izzo et al. (2001) [29]	26	1.8 (0.7–3.0)	57 (37–78)^1	LeVeen	96% (NADH)	Immediately	Skin burn (1)	15.4 (6.4 – 24.9)
Burak et al. (2003) [46]	10	1.2 (0.8–1.6)	53.7 (37–67)	RadioTherapeutics	90% (H&E)	16.1 (8–24) D	Ecchymosis (1)	13.8 (7–21)
Hayashi et al. (2003) [27]	22	0.9 (0.5–2.6)^1	73 (60–80)^1	StarBurst	86% (NADH, H&E)	1–2 wk	Skin burn (1), Ecchymosis (2)	15 (15–20.5)^1
Singletary (2003) [26]	29	<2.0	–	RITA Model 500/Starburst	86% (NADH, H&E)	Immediately	Skin burn (1)	30–45
Fornage et al. (2004) [45]	20 (21)	1.2 ± 0.3 (0.6–2.0)	56 ± 11 (38–80)	StarBurst	100% (NADH)	Immediately		21.2 (18.9–29)
Noguchi et al. (2006) [13]	10	1.1 (0.5–2.0)	54 (33–70)	StarBurst	100% (NADH)	Immediately	–	18 (17–19.5)
Earashi et al. (2007) [65]	17 + 7	1.1 (0.5–2.4) and 1.1 (0.7–2.0)	55 (33–78) and 44 (29–55)	StarBurst	100% (NADH)	Immediately (n = 17), delayed (n = 7) by mammotome 91 (30–202) D^1	–	18 (17–21.5)
Khatri et al. (2007) [44]	15	1.3 (0.8–1.5)	63 (39–83)	Cool-Tip	93% (NADH)	Immediately	Skin puckering (2), infection (1)	21 (7–36)
Oura et al. (2007) [66]	52	1.3 (0.5–2.0)	55 (37–83)	Cool-Tip	100% (CNB)	Follow-up 15 (6–30) M	Skin burn (1)	12 (5–25)
Garbay et al. (2008) [43]	10	1.4 (1.0–2.2)^1	50 (44–70)^1	LeVeen	75% (NADH, n = 8), 70% (H&E, n = 10)	Immediately	–	10.7 (5.3–16.0)
Medina-Franco et al. (2008) [42]	25	2.1 (0.9–3.8)	55.3 (42–89)	Elektrotom	76% (NADH)	Immediately	Skin burn (3), skin infection (1), recurrence (2)	11 (9–15)
Imoto et al. (2009) [14]	30	1.7 (0.9–2.4)^1	38–76	LeVeen	92% (NADH), 87% (H&E)	Immediately	Skin burn (2, incl skin necrosis (1)), pectoralis major burn (7)	18 (4–42)
Manenti et al. (2009) [22]	34	1.9 ± 0.6 (1.7–2.0)	53 ± 5 (49–62)	Cool-Tip	97% (NADH)	4 wk	Skin burn (1)	27 ± 3.7 (25–35)
Nagashima et al. (2009) [38]	17	1.1 (0.6–1.8)	61.8 (47–71)	Cool-Tip	100% (imaging)	Follow-up 19 M (12–28)^1	–	9.6 (6.5–17)
Motoyoshi et al. (2010) [69]	2 × 17	1.5 (0.5–2.1) and 1.2 (0.5–2.0)	55 (33–78)^1 and 45 (22–59)^1	StarBurst	100% (NADH, n = 33), 64.7% (H&E, n = 34)	Immediately,delayed 30–202 D	Recurrence (3)	–
Wiksell et al. (2010) [15]	31	1.1 ± 0.3 (0.6–1.5)	63.6 ± 8.9 (46–83)	NeoDynamics AB	84% (H&E)	Immediately	Skin burn (1), muscle burn (2), pneumothorax (1)	9.5 ± 1.2 (6.5–11)
Hung et al. (2011) [51]	2 × 10	1.4 ± 0.3 vs. 1.3 ± 0.3	60 ± 12 vs. 57 ± 9	LeVeen and Cool-Tip	90% and 89% (H&E, NADH)	Immediately	Blistering (5), coagulative changes to skin (n = 4)	28 ± 6 vs. 12 ± 0
Kinoshita et al. (2011) [48]	49	1.7 (0.5–3.0)	61 (36–82)^1	Cool-Tip	61% (H&E and NADH)	Immediately	Skin burn (2), muscle burn (3)	8.7 (3–18)
Ohtani et al. (2011) [16]	41	1.3 (0.6–3.5)^1	59 (38–92)^1	Cool-Tip	87.8% (H&E, NADH)	Immediate (n = 9), delayed 1–2 M (n = 32)	Skin burn (1)	9 (6–15)^1
Tsuda et al. (2011) [71]	28	2.2 ± 1.3 (0.6–5.0)	59.1 (36–82)	Cool-Tip	79% (NADH)	Immediately	–	–
Yamamoto et al. (2011) [30]	29 (30)	1.3 (0.5–1.9)	55.9 (38–78)	Cool-Tip	92% (NADH, n = 26)	Follow-up17 (2–41) M	Skin burn (3), overreaction (1)	11.4 (6–20)
Noguchi et al. (2012) [70]	19	1.3 (0.5–2.0)^1	45 (22–59)^1	StarBurst	100% (NADH, n = 18)	30 (24–202)D^1	–	15
Palussiere et al. (2012) [31]	21	2.0^1	79 (70–88)^1	LeVeen	–	Follow-up 49.6 (17–77)M^1	Skin burn (4), nipple retraction (3), recurrence (3)	11 (4–19)
Vilar et al. (2012) [47]	14	1.8 (1.0–2.5)	56 (37–71)	LeVeen	50% (H&E)	3 wk	skin burn (1), fistula (1)	–
Manenti et al. (2013) [53]	40	–	73 ± 5 (64–82)	Miras PTV	92.5% (H&E, NADH)	34 (30–45) D	–	27 (24–35)
Yoshinaga et al. (2013) [32]	6 + 8	1.2 (0.6–2.0)^1	67 (45–82)^1	Cool-Tip	100% (n = 7), 100% (NADH, n = 5)	Immediate (n = 6), follow-up 39.9 M (n = 8)^1	Skin burn (1)	9.6 (4.8–14.7)^1
Schassburger et al. (2014) [17]	18	1.0 (0.6–1.5)^1	67 (46–84)^1	NeoDynamics	89% (CK8)	14.5 (6–22) D^1	–	10 (8–14)^1
Waaijer et al. (2014) [34]	15	1.1 (0.4–1.7)^1	63 (50–76)^1	CelonProSurge	77% (n = 13)	Immediately	Pneumothorax (1), recurrence (1)	13 ± 0.2 (6–26)

CA: complete ablation; CK8: cytokeratine 8; d: days; H&E: haematoxylin and eosin; m: months; min: minutes; N: number of patients; NADH: nicotinamide adenine dinucleotide; wk: weeks; yr: years.

* Values are mean ± SD (range), unless indicated otherwise by ¹ in which case it is medium (range).

+ Cool-Tip RF Needle Electrode (Radionics, Burlington, MA); Elektrotom 106 HiTT (Berchtold, Germany); LeVeen needle electrode (RadioTherapeutics Corporation, Mountain View, CA); Miras PTV (University Hospital Policlinico Tor Vergata, Rome, Italy and INVATEC ITALIA, Roncadelle, Brescia, Italy); unknown model type (NeoDynamics AB, Sweden); StarBurst radioprobe (RITA Medical Systems, Mountain View, California); bipolar radiofrequency ablation system was used (CelonProSurge150-T20, Olympus Winter & Ibe GmbH, Hamburg, Germany).

Table 2. Quality assessment (yes/no) for (a) cohort studies and (b) randomised controlled trials.

			Standardised
(a)	Objective	Incl. criteria	Technique	Histopathology	Imaging	Follow-up	Withdrawals
Radiofrequency ablation	27/0	26/1	25/2	27/0	11/3 (13 –)	12/15	0/27
Cryo-ablation	10/0	8/2	9/1	9/1	4/1 (5 –)	3/7	2/8
Laser ablation	7/0	4/3	7/0	6/1	3/2 (2 –)	3/4	1/6
HIFU	10/0	9/1	8/2	5/5	10/0	3/7	3/7
Microwave ablation	4/0	3/1	4/0	4/0	1/0 (3 –)	0/4	0/4
Combined technique	1/0	1/0	1/0	1/0	1/0	0/1	0/1

Study quality was assessed according to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement.

– no data available to answer.

Table 1(b). Study characteristics and outcomes for laser ablation.

Study	N	Size (cm)*	Age (yr)*	Device^+	CA	Complications	Resection*	Time (min)*
Harries et al. (1994) [28]	44	–	–	Diomed	–	Haemorrhage (1)	1–34 D	3.3–12.5
Mumtaz et al. (1996) [50]	20 (27)	2.0 (0.4–3.3)^1	57 (34–79)^1	Diomed	–	–	5 (1–15) D^1	5.0–8.3
Akimov et al. (1998) [33]	28 + 7	3.0 (1.0–6.0)^1	53 (38–78)^1	Nd:YAG	–	Gaseous rupture of the tumour (1), skin burn (4), recurrence (9)	Delayed (n = 28) 1–11 D, follow-up (n = 7) 20.5 (5–64) M	–
Bloom et al. (2001) [62]	40	0.95 (0.5–2.3)	60 (42–80)	Diomed	–	–	14.5 (0–70) D	–
Dowlatshahi et al. (2002) [63]	54	1.3 (0.5–2.3)	60 (42–80)	Diomed	70%	Skin burn (2)	1–8 wk	25–30
Haraldsdottir et al. (2008) [34]	24	1.4 (0.5–3.5)	61 (39–84)	Diomed	12.5% (H&E)	Skin necrosis (2), recurrence (2)	12 (4–23) D	30
Van Esser et al. (2009) [18]	14	1.7 (0.8–3.7)^1	54.5 (35–85)^1	Nd:YAG	50% (NADH)	Skin burn (1), pneumothorax (1)	Immediately	21.4 (15–30)

CA: complete ablation; d, days; H&E: haematoxylin and eosin; m: months; min: minutes; N: number of patients; NADH: nicotinamide adenine dinucleotide; wk: weeks; yr: years.

* Values are mean ± SD (range), unless indicated otherwise by ¹ in which case it is medium (range).

+ Diomed (Cambridge, UK); Nd:YAG laser (Polar Ltd., Russia).

Table 1(c). Study characteristics and outcomes of cryo-ablation.

Study	N	Size (cm)*	Age (years)*	Device type^+	CA	Complications	Resection*	Time (min)*
Pfleiderer et al. (2002) [19]	15 (16)	2.2 ± 0.93 (0.9–4.0)	60.3 ± 9.4 (38–80)	CryoHit	31.3%	Seroma (1)	1–5 D	52.4 ± 7.1 (41–64)
Tafra et al. (2003) [35]	24	1.2 ± 0.4 (0.7–2.0)	61 (41–78)	Visica	–	–	Immediately	15.8 ± 7.6 (14^1)
Sabel et al. (2004) [36]	29	1.2 ± 0.5 (0.6–2.0)	52.5 (34–77)^1	Visica	85% (H&E, n = 27)	–	14 (6–30) D	30
Morin et al. (2004) [37]	25	3.0 (1.2–6.0)	61.0 (41–77)	CryoHit	52%	Minimal skin burn (?) and mastitis (?)	4 wk	180
Pfleiderer et al. (2005) [20]	30	1.2 (0.5–1.5)^1	61.5 (48–80)^1	CryoHit	83% (H&E)	Arterial bleeding (1), seroma (1)	11 ± 9.2 D	40–75
Pusztaszeri et al. (2007) [61]	11	1.3 (0.5–2.5)	63 (52–78)	CryoHit	20% (H&E)	Skin ulceration and/or necrosis (5)	4–5 wk	20
Littrup et al. (2009) [21]	11 (18 + 4 LN)	1.7 ± 1.2 (0.5–5.8)	62.5	Endocare	100% (CNB, n = 6)	–	Follow-up 22.8 M	24.7 (14–33)
Manenti et al. (2011) [22]	15	0.8 ± 0.4 (4–1.2)	73 ± 5 (64–82)	IceRod^®	93.3% (H&E)	Subcutaneous haematoma (2), ecchymosis (4)	34 (30–45) D	–
Manenti et al. (2013) [53]	40	–	73 ± 5 (64–82)	IceRod^®	95% (H&E, NADH)	–	34 (30–45) D	–
Cazatto et al. (2015) [73]	23	1.4 (0.5–2.8)^1	85 (56–96)^1	IceSphere and IceRod^®	–	Haematoma (3), skin burn to imflammation to skin retraction (1), haematoma to skin retraction (1), skin retraction to ulceration (1), recurrence (n = 1)	Follow-up 14.6 M^1	29.4
Simmons et al. (2016) [49]	86 (87)	1.2 ± 0.3 (0.5–1.9)	61.1 ± 9.3 (42–81)	Visica	75.9% (H&E)	–	<4 wk	–

CA: complete ablation; d: days; H&E: haematoxylin and eosin; m: months; min: minutes; N: number of patients; NADH: nicotinamide adenine dinucleotide; wk: weeks; yr: years.

* Values are mean ± SD (range), unless indicated otherwise by ¹ in which case it is medium (range).

+ CryoHit (Galil Medical, Yokneam, Israel); Endocare, (Irvine, California); IceRod® and IceSphere models (Galil Medical, Yokneam, Israel); Visica Cryoablation System (Sanarus Medical, Inc., Pleasanton, CA).

Table 1(d). Study characteristics and outcomes for high intensity focussed ultrasound (HIFU).

Study	n	Size (cm)*	Age (years)*	Guidance and device^+	CA	Resection*	Complications	Time (min)*
Gianfelice et al. (2003) [57]	12	2.8 (0.1–8.8) cm^3	60 ± 9.6 (45–74)	MRI, ExAblate 2000	17% (H&E)	Delayed (unknown time)	Skin burn (2)	80 (35–133)
Gianfelice et al. (2003) [23]	17	2.5 (0.1–8.8) cm^3	61.2 ± 8.9 (48–76)	MRI, ExAblate 2000	24% (H&E)	3–21 D	–	–
Gianfelice et al. (2003) [23]	24	1.5 (0.6–2.5)	74.2 (53–92)	MRI, ExAblate 2000	79%	Follow-up 20.2 M (12–39)	Skin burn (1)	–
Wu et al. (2003) [55]	23	3.1 ± 0.8 (2.0–4.7)	46.5 ± 1.7	US, JC HAIFU	100% (H&E)	1–2 wk	Skin burn (1)	78 (45–150)^1
Wu et al. (2005) [23]	22	3.4 (2.0–4.8)	48.6 (36–68)	US, JC HAIFU	100% (H&E)	Follow-up 54.8 M (36–72)^1	Recurrence (2)	132 (60–180)^1
Zippel and Papa (2005) [38]	10	2.2	56 (45–72)	MRI, ExAblate 2000	20%	7–10 D	Skin burn (1)	Max 240
Khiat et al. (2006) [59]	25 (26)	3.3 (0.1–11.2) cm^3	61.3 ± 11 (45–87)	MRI, ExAblate 2000	31% (8/26)	3–21 D	–	–
Furusawa et al. (2006) [8]	28	1.3 (0.5–2.5)	56.9 (41–79)	MRI, ExAblate 2000	53.5% (H&E)	5–23 D	Skin burn (1)	140 (76–231)
Furusawa et al. (2007) [60]	21	1.5 (0.5–5.0)^1	54 (34–72)^1	MRI, ExAblate 2000	–	Follow-up 14 M (3–26)	Skin burn (2), recurrence (1)	–
Cavallo-Marincola et al. (2013) [52]	10	1.2	–	MRI, Exablate 2100	60%	24–35 D	–	140 (80–180)
Merckel et al. (2016) [72]	10	2.0 ± 0.6	54.8 ± 12.5	MRI, Sonalleve	–	5.0 ± 2.2 D	White lumps (1)	46 ± 17 (12–75)
Guan and Xu (2016) [56]	25	(2.1–4.8)	48 (22–63)	US, JC HAIFU	–	1–2 wk	Fever (3)	66 (40–132)^1

CA: complete ablation; d: days; H&E : haematoxylin and eosin; m: months; min : minutes; N : number of patients; NADH : nicotinamide adenine dinucleotide; wk: weeks; yr : years.

* Values are mean ± SD (range), unless indicated otherwise by ¹ in which case it is medium (range).

+ JC HAIFU (Chongqing Haifu Tech Co., Ltd., China**); ExAblate 2000; InSightec-TxSonics, Haifa, Israel and Dallas, TX); Sonalleve (Philips Healthcare, Finland).

Table 1(e). Study characteristics and outcomes for microwave ablation.

Study	N	Size (cm)*	Age (years)*	Device^+	CA	Complications	Resection*	Time (min)*
Gardner et al. (2002) [39]	10	4.3 (1–8)	58.5 (47–82)	Medifocus 1000 APA	–	Flap necrosis (3), blister (1)	5–27 D	34.7 (12–40)
Vargas et al. (2004) [41]	25	1.76 (0.7–2.8)	57.2	Medifocus 1000 APA	68% (H&E)	Skin burn (3)	17 (6–38) D	–
Dooley et al. (2010) [54]	41	1.6 (0.7–2.73)	58.0	Medifocus 1000 APA	85.3% (H&E)	Skin burn (3), nipple retraction (1), seroma (6), abscess (1)	19.6 (7–60) D	–
Dooley et al. (2010) [54]	15	3.65 (2.0–7.8)	45.1 (26–72)	Medifocus 1000 APA	–	Skin burn (5 treatments)	Delayed (unknown)	34.8
Zhou et al. (2012) [25]	41	2.0 ± 0.5 (1.0–3.0)	55.5 ± 11.4 (38–78)	–	90% (NADH)	Skin injury (1), pectoralis major injury (2)	Immediate	4.48 ± 2.03 (3–10)
Zhou et al. (2014) [40]	12	2.89 ± 0.44	54 (34–61)^1	–	–	–	>3 wk	2.15 (1.3–3)

CA: complete ablation; d: days; H&E: haematoxylin and eosin; m: months; min: minutes; N: number of patients; NADH: nicotinamide adenine dinucleotide; wk: weeks: yr: years.

* Values are Mean ± SD (range), unless indicated otherwise by ¹ in which case it is medium (range).

+ Medifocus-1000 APA (Celsion Corporation, Columbia, MD).

Figure 2. Probabilities of success to achieve complete pathological response with 95% confidence intervals calculated using a random logistic effect model. RFA: radiofrequency ablation; LASER: laser ablation; CRYO: cryo-ablation; HIFU: high intensity focused ultrasound; MW: microwave ablation.

Izzo F, Thomas R, Delrio P, et al. (2001). Radiofrequency ablation in patients with primary breast carcinoma: a pilot study in 26 patients. Cancer 92:2036–44.

 PubMed Web of Science ®Google Scholar

Burak WE Jr, Agnese DM, Povoski SP, et al. (2003). Radiofrequency ablation of invasive breast carcinoma followed by delayed surgical excision. Cancer 98:1369–76.

 PubMed Web of Science ®Google Scholar

Hayashi AH, Silver SF, Van Der Westhuizen NG, et al. (2003). Treatment of invasive breast carcinoma with ultrasound-guided radiofrequency ablation. Am J Surg 185:429–35.

 PubMed Web of Science ®Google Scholar

Singletary ES. (2003). Feasibility of radiofrequency ablation for primary breast cancer. Breast Cancer 10:4–9.

 PubMedGoogle Scholar

Fornage BD, Sneige N, Ross MI, et al. (2004). Small (< or =2-cm) breast cancer treated with US-guided radiofrequency ablation: feasibility study. Radiology 231:215–24.

 PubMed Web of Science ®Google Scholar

Noguchi M, Earashi M, Fujii H, et al. (2006). Radiofrequency ablation of small breast cancer followed by surgical resection. J Surg Oncol 93:120–8.

 PubMed Web of Science ®Google Scholar

Earashi M, Noguchi M, Motoyoshi A, Fujii H. (2007). Radiofrequency ablation therapy for small breast cancer followed by immediate surgical resection or delayed mammotome excision. Breast Cancer 14:39–47.

 PubMedGoogle Scholar

Khatri VP, Mcgahan JP, Ramsamooj R, et al. (2007). A phase II trial of image-guided radiofrequency ablation of small invasive breast carcinomas: use of saline-cooled tip electrode. Ann Surg Oncol 14:1644–52.

 PubMed Web of Science ®Google Scholar

Oura S, Tamaki T, Hirai I, et al. (2007). Radiofrequency ablation therapy in patients with breast cancers two centimetres or less in size. Breast Cancer 14:48–54.

 PubMedGoogle Scholar

Garbay JR, Mathieu MC, Lamuraglia M, et al. (2008). Radiofrequency thermal ablation of breast cancer local recurrence: a phase II clinical trial. Ann Surg Oncol 15:3222–6.

 PubMed Web of Science ®Google Scholar

Medina-Franco H, Soto-Germes S, Ulloa-Gomez JL, et al. (2008). Radiofrequency ablation of invasive breast carcinomas: a phase II trial. Ann Surg Oncol 15:1689–95.

 PubMed Web of Science ®Google Scholar

Imoto S, Wada N, Sakemura N, et al. (2009). Feasibility study on radiofrequency ablation followed by partial mastectomy for stage I breast cancer patients. Breast 18:130–4.

 PubMed Web of Science ®Google Scholar

Manenti G, Perretta T, Gaspari E, et al. (2011). Percutaneous local ablation of unifocal subclinical breast cancer: clinical experience and preliminary results of cryotherapy. Eur Radiol 21:2344–53.

 PubMed Web of Science ®Google Scholar

Zippel DB, Papa MZ. (2005). The use of MR imaging guided focused ultrasound in breast cancer patients; a preliminary phase one study and review. Breast Cancer 12:32–8.

 PubMedGoogle Scholar

Motoyoshi A, Noguchi M, Earashi M, et al. (2010). Histopathological and immunohistochemical evaluations of breast cancer treated with radiofrequency ablation. J Surg Oncol 102:385–91.

 PubMed Web of Science ®Google Scholar

Wiksell H, Lofgren L, Schassburger KU, et al. (2010). Feasibility study on the treatment of small breast carcinoma using percutaneous US-guided preferential radiofrequency ablation (PRFA). Breast 19:219–25.

 PubMed Web of Science ®Google Scholar

Hung WK, Mak KL, Ying M, Chan M. (2011). Radiofrequency ablation of breast cancer: a comparative study of two needle designs. Breast Cancer 18:124–8.

 PubMed Web of Science ®Google Scholar

Kinoshita T, Iwamoto E, Tsuda H, Seki K. (2011). Radiofrequency ablation as local therapy for early breast carcinomas. Breast Cancer 18:10–17.

 PubMed Web of Science ®Google Scholar

Ohtani S, Kochi M, Ito M, et al. (2011). Radiofrequency ablation of early breast cancer followed by delayed surgical resection – a promising alternative to breast-conserving surgery. Breast 20:431–6.

 PubMed Web of Science ®Google Scholar

Tsuda H, Seki K, Hasebe T, et al. (2011). A histopathological study for evaluation of therapeutic effects of radiofrequency ablation in patients with breast cancer. Breast Cancer 18:24–32.

 PubMed Web of Science ®Google Scholar

Yamamoto N, Fujimoto H, Nakamura R, et al. (2011). Pilot study of radiofrequency ablation therapy without surgical excision for T1 breast cancer: evaluation with MRI and vacuum-assisted core needle biopsy and safety management. Breast Cancer 18:3–9.

 PubMed Web of Science ®Google Scholar

Noguchi M, Motoyoshi A, Earashi M, Fujii H. (2012). Long-term outcome of breast cancer patients treated with radiofrequency ablation. Eur J Surg Oncol 38:1036–42.

 PubMed Web of Science ®Google Scholar

Palussiere J, Henriques C, Mauriac L, et al. (2012). Radiofrequency ablation as a substitute for surgery in elderly patients with nonresected breast cancer: pilot study with long-term outcomes. Radiology 264:597–605.

 PubMed Web of Science ®Google Scholar

Vilar VS, Goldman SM, Ricci MD, et al. (2012). Analysis by MRI of residual tumor after radiofrequency ablation for early stage breast cancer. AJR Am J Roentgenol 198:W285–91.

 PubMed Web of Science ®Google Scholar

Manenti G, Scarano AL, Pistolese CA, et al. (2013). Subclinical breast cancer: minimally invasive approaches. Our experience with percutaneous radiofrequency ablation vs. Cryotherapy. Breast Care (Basel) 8:356–60.

 PubMed Web of Science ®Google Scholar

Yoshinaga Y, Enomoto Y, Fujimitsu R, et al. (2013). Image and pathological changes after radiofrequency ablation of invasive breast cancer: a pilot study of nonsurgical therapy of early breast cancer. World J Surg 37:356–63.

 PubMed Web of Science ®Google Scholar

Schassburger KU, Lofgren L, Leifland K, et al. (2014). Minimally-invasive treatment of early stage breast cancer: A feasibility study using radiofrequency ablation under local anaesthesia. Breast 23:152–8. doi:10.1016/j.breast.2013.12.007.

 Google Scholar

Haraldsdottir KH, Ivarsson K, Gotberg S, et al. (2008). Interstitial laser thermotherapy (ILT) of breast cancer. Eur J Surg Oncol 34:739–45.

 PubMed Web of Science ®Google Scholar

Harries SA, Amin Z, Smith ME, et al. (1994). Interstitial laser photocoagulation as a treatment for breast cancer. Br J Surg 81:1617–9.

 PubMed Web of Science ®Google Scholar

Mumtaz H, Hall-Craggs MA, Wotherspoon A, et al. (1996). Laser therapy for breast cancer: MR imaging and histopathologic correlation. Radiology 200:651–8.

 PubMed Web of Science ®Google Scholar

Akimov AB, Seregin VE, Rusanov KV, et al. (1998). Nd: YAG interstitial laser thermotherapy in the treatment of breast cancer. Lasers Surg Med 22:257–67.

 PubMed Web of Science ®Google Scholar

Bloom KJ, Dowlat K, Assad L. (2001). Pathologic changes after interstitial laser therapy of infiltrating breast carcinoma. Am J Surg 182:384–8.

 PubMed Web of Science ®Google Scholar

Dowlatshahi K, Francescatti DS, Bloom KJ. (2002). Laser therapy for small breast cancers. Am J Surg 184:359–63.

 PubMed Web of Science ®Google Scholar

Van Esser S, Stapper G, Van Diest PJ, et al. (2009). Ultrasound-guided laser-induced thermal therapy for small palpable invasive breast carcinomas: a feasibility study. Ann Surg Oncol 16:2259–63.

 PubMed Web of Science ®Google Scholar

Pfleiderer SO, Freesmeyer MG, Marx C, et al. (2002). Cryotherapy of breast cancer under ultrasound guidance: initial results and limitations. Eur Radiol 12:3009–14.

 PubMed Web of Science ®Google Scholar

Tafra L, Smith SJ, Woodward JE, et al. (2003). Pilot trial of cryoprobe-assisted breast-conserving surgery for small ultrasound-visible cancers. Ann Surg Oncol 10:1018–24.

 PubMed Web of Science ®Google Scholar

Sabel MS, Kaufman CS, Whitworth P, et al. (2004). Cryoablation of early-stage breast cancer: work-in-progress report of a multi-institutional trial. Ann Surg Oncol 11:542–9.

 PubMed Web of Science ®Google Scholar

Morin J, Traore A, Dionne G, et al. (2004). Magnetic resonance-guided percutaneous cryosurgery of breast carcinoma: technique and early clinical results. Can J Surg 47:347–51.

 PubMed Web of Science ®Google Scholar

Pfleiderer SO, Marx C, Camara O, et al. (2005). Ultrasound-guided, percutaneous cryotherapy of small (< or =15 mm) breast cancers. Invest Radiol 40:472–7.

 PubMed Web of Science ®Google Scholar

Pusztaszeri M, Vlastos G, Kinkel K, Pelte MF. (2007). Histopathological study of breast cancer and normal breast tissue after magnetic resonance-guided cryotherapy ablation. Cryobiology 55:44–51.

 PubMed Web of Science ®Google Scholar

Littrup PJ, Jallad B, Chandiwala-Mody P, et al. (2009). Cryotherapy for breast cancer: a feasibility study without excision. J Vasc Interv Radiol 20:1329–41.

 PubMed Web of Science ®Google Scholar

Cazzato RL, De Lara CT, Buy X, et al. (2015). Single-centre experience with percutaneous cryoablation of breast cancer in 23 consecutive non-surgical patients. Cardiovasc Interv Radiol 38:1237–43.

 PubMed Web of Science ®Google Scholar

Simmons RM, Ballman KV, Cox C, et al. (2016). A phase II trial exploring the success of cryoablation therapy in the treatment of invasive breast carcinoma: results from ACOSOG (Alliance) Z1072. Ann Surg Oncol 23:2438–45. doi:10.1245/s10434-016-5275-3.

 PubMed Web of Science ®Google Scholar

Gianfelice D, Khiat A, Amara M, et al. (2003). MR imaging-guided focused US ablation of breast cancer: histopathologic assessment of effectiveness-initial experience. Radiology 227:849–55.

 PubMed Web of Science ®Google Scholar

Gianfelice D, Khiat A, Boulanger Y, et al. (2003). Feasibility of magnetic resonance imaging-guided focused ultrasound surgery as an adjunct to tamoxifen therapy in high-risk surgical patients with breast carcinoma. J Vasc Interv Radiol 14:1275–82.

 PubMed Web of Science ®Google Scholar

Wu F, Wang ZB, Cao YD, et al. (2003). A randomised clinical trial of high-intensity focused ultrasound ablation for the treatment of patients with localised breast cancer. Br J Cancer 89:2227–33.

 PubMed Web of Science ®Google Scholar

Khiat A, Gianfelice D, Amara M, Boulanger Y. (2006). Influence of post-treatment delay on the evaluation of the response to focused ultrasound surgery of breast cancer by dynamic contrast enhanced MRI. Br J Radiol 79:308–14.

 PubMed Web of Science ®Google Scholar

Furusawa H, Namba K, Thomsen S, et al. (2006). Magnetic resonance-guided focused ultrasound surgery of breast cancer: reliability and effectiveness. J Am Coll Surg 203:54–63.

 PubMed Web of Science ®Google Scholar

Furusawa H, Namba K, Nakahara H, et al. (2007). The evolving non-surgical ablation of breast cancer: MR guided focused ultrasound (MRgFUS)). Breast Cancer 14:55–8.

 PubMedGoogle Scholar

Cavallo Marincola B, Pediconi F, Anzidei M, et al. (2015). High-intensity focused ultrasound in breast pathology: non-invasive treatment of benign and malignant lesions. Expert Rev Med Dev 12:191–9.

 PubMed Web of Science ®Google Scholar

Merckel LG, Knuttel FM, Deckers R, et al. (2016). First clinical experience with a dedicated MRI-guided high-intensity focussed ultrasound system for breast cancer ablation. Eur Radiol. [Epub ahead of print]. doi:10.1007/s00330-016-4222-9.

 PubMed Web of Science ®Google Scholar

Guan L, Xu G. (2016). Damage effect of high-intensity focused ultrasound on breast cancer tissues and their vascularities. World J Surg Oncol 14:153.

 PubMed Web of Science ®Google Scholar

Gardner RA, Vargas HI, Block JB, et al. (2002). Focused microwave phased array thermotherapy for primary breast cancer. Ann Surg Oncol 9:326–32.

 PubMed Web of Science ®Google Scholar

Vargas HI, Dooley WC, Gardner RA, et al. (2004). Focused microwave phased array thermotherapy for ablation of early-stage breast cancer: results of thermal dose escalation. Ann Surg Oncol 11:139–46.

 PubMed Web of Science ®Google Scholar

Dooley WC, Vargas HI, Fenn AJ, et al. (2010). Focussed microwave thermotherapy for preoperative treatment of invasive breast cancer: a review of clinical studies. Ann Surg Oncol 17:1076–93.

 PubMed Web of Science ®Google Scholar

Zhou W, Zha X, Liu X, et al. (2012). US-guided percutaneous microwave coagulation of small breast cancers: a clinical study. Radiology 263:364–73.

 PubMed Web of Science ®Google Scholar

Zhou W, Jiang Y, Chen L, et al. (2014). Image and pathological changes after microwave ablation of breast cancer: a pilot study. Eur J Radiol 83:1771–7.

 PubMed Web of Science ®Google Scholar