Ablative margins in percutaneous thermal ablation of hepatic tumors: a systematic review

Figures & data

Figure 1. Preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) flow diagram describing the results of the systematic literature search and additional selection based on exclusion criteria. LTP = local tumor progression.

Table 1. Characteristics of articles included in this review. NR = not reported; PS = prospective; RS = retrospective; RFA = radiofrequency ablation; MWA = microwave ablation; LTP = local tumor progression; HCC = hepatocellular carcinoma; CRLM = colorectal liver metastases; AM = ablative margin; 3D-QAM = three-dimensional quantitative ablative margin; NLR = neutrophil-lymphocyte ratio, 3D-CEUS-FI = three-dimensional contrast enhanced ultrasound fusion imaging.

Reference	Year	Country	Study design	Ablation	Patients (lesions)	Tumor type	Tumor size (cm)	Factor influencing LTP
An et al. [33]	2020	China	PS	MWA	141	HCC	2.3 ± 0.9	Older age (HR = 2.463; 95% CI: 1.028, 6.152; p = .032) and an AM ≤5 mm (HR = 3.195; 95% CI: 1.324–7.752; p = .010)
An et al. [34]	2019	China	RS	MWA	68	HCC	3.4 ± 0.6	Maximal tumor diameter (HR = .923; p = .006) and tumor map (HR = .716; p = .003)
Bo et al. [35]	2017	China	RS	RFA	34 (47)	Mixed	2.0 ± 1.0	NR
Du et al. [36]	2022	China	PS	MWA	31 (42)	HCC	NR	NR
Faber et al. [37]	2022	The Netherlands	RS	RFA	21 (29)	CRLM	2.05	Uncovered tumor volume (622 mm3 (IQR 471–2246)) vs. (123 mm3 (IQR 11–230); p = .010);
Fukuda et al. [38]	2019	Japan	PS	RFA	76 (85)	HCC	1.5 (0.8–3.0)	NR
Hendriks et al. [39]	2019	The Netherlands	RS	RFA	18	HCC	2.2 (1.2–1.7)	AM size (p = .001)
Hocquelet et al. [40]	2017	France	RS	RFA	16	HCC	2.9	Margins >425 mm2 (HR = 6.71,95% CI: 1.27–35.5; p = .014)
Inoue et al. [41]	2013	Japan	PS	RFA	70 (86)	HCC	1.7 ± 0.7	NR
Izaaryene et al. [42]	2021	France	RS	MWA	84	CRLM	1.5 ± 0.8	Presence of a colonic obstruction or a perforation at the time of initial diagnosis (p < .05), the number of metastases at the time of diagnosis (p < .05), the number of surgical resections of liver metastases before MWA (p < .05), the type of protocol (p < .05), and ablative margins (p < .001)
Jiang et al. [43]	2018	China	RS	RFA	134 (159)	HCC	2.0 ± 0.9	min-AM <5 mm (HR = 4.587, 95% CI: 1.045–22.296; p = .044).
Joo et al. [44]	2022	USA	RS	MWA	172 (334)	Mixed	1.85 ± 0.89	Insufficient ablative margin on post-MWA MRI (HR = 14.39, 95% CI: 4.61–44.92: p < .001), perivascular tumor location (HR = 6.03, 95% CI: 1.83–19.87: p = .003), and tumor size (HR = 1.0, 95% CI: 1.01–1.11: p = .011)
Kaye et al. [45]	2019	USA	RS	RFA	72 (93)	CRLM	1.8	5-mm metric highest 2-year LTP discrimination power, AUC = .923 (p = .004)
Ke et al. [46]	2014	China	PS	RFA	281	HCC	4.1	AM >1.0 cm (HR = 1.484, 95% CI: .101–1.812; p = .001)
Kim et al. [47]	2018	South Korea	PS	RFA	33 (42)	HCC	1.58 ± 0.59	NR
Laimer et al. [48]	2021	Austria	RS	RFA	45 (76)	CRLM	2.42	Peri-ablational 3D safety margin (p < .001)
Laimer et al. [49]	2020	Austria	RS	RFA	110 (176)	HCC	2.52 ± 1.49	Minimum AM (p = .036)
Li et al. [50]	2021	China	RS	RFA/MWA	444	HCC	1.9	Tumor size (HR = 2.16; 95% CI: 1.25–3.72; p = .003) and AM (HR = .72; 95% CI: .61–.85; p < .001)
Li et al. [51]	2016	China	PS	RFA	98 (126)	HCC	1.96 ± 0.77	AM (HR = 9.167, 95% CI: 1.070–78.571; p = .043)
Makino et al. [52]	2013	Japan	RS	RFA	85 (94)	HCC	1.4 ± 0.52	Protrusion from the ablation zone (HR = 7.09, 95% CI: 2.26–22.3; p < .001)
Makino et al. [53]	2016	Japan	RS	RFA	69 (85)	HCC	1.19	NR
Matsuki et al. [54]	2021	Japan	PS	RFA	42 (48)	HCC	1.32	NR
Minami et al. [55]	2020	Japan	RS	RFA	101 (121)	HCC	1.8 ± 0.7	NR
Park et al. [56]	2018	South Korea	RS	RFA	178 (178)	HCC	1.73 ± 0.61	NR
Ruiter et al. [57]	2021	The Netherlands	RS	MWA	47 (65)	CRLM	1.3	3D-QAM (OR = .52, CI .29–.95; p = .03)
Sakakibara et al. [58]	2014	Japan	RS	RFA	84 (133)	HCC	1.38 ± 0.46	NR
Sanga et al. [59]	2020	Japan	PS	RFA	43 (5)	HCC	1.53	NR
Shady et al. [60]	2018	USA	RS	RFA/MWA	110 (145)	CRLM	NR	RFA: ablative margin <5 mm (p < .001) and peri-vascular location (p < .001)MWA: ablative margin <5 mm (p < .001) and no prior liver resection (p = .002) MWA: ablative margin <5 mm (p < 0.001) and no prior liver resection (p = 0.002)
Shin et al. [61]	2014	South Korea	PS	RFA	240	HCC	1.95 ± 0.79	Visual vs. CT margin assessment (p = .0101)
Sibinga Mulder et al. [27]	2019	The Netherlands	RS	RFA	18	CRLM	2.2	NR
Solbiati et al. [62]	2019	Italy	RS	MWA	50 (90)	HCC	2.7 ± 2	NR
Sparchez et al. [63]	2019	Romania	RS	RFA/MWA	61 (82)	Mixed	2.5	Ablative margin ≤5 mm (p = .002) and tumor number (p = .049)
Takeyama et al. [64]	2019	Japan	RS	RFA	29 (59)	HCC	1.12 ± 0.44	Ablative margin status (p = .028)
Tang et al. [65]	2015	China	PS	RFA	75	HCC	2.4 ± 0.7	Pre-operative NLR (HR: 2.34, 95% CI: 1.11–5.12; P = .026), AM change (HR = 2.15, 95% CI: 1.01–4.60; p = .048)
Tokunaga et al. [66]	2012	Japan	PS	RFA	45 (60)	HCC	1.68 ± 0.59	NR
Toshikuni et al. [67]	2017	Japan	PS	RFA	45 (45)	HCC	1.9	NR
Vasiniotis Kamarinos et al. [68]	2022	USA	RS	RFA	68 (104)	CRLM	1.9	NR
Wang et al. [69]	2016	China	PS	RFA	51 (61)	HCC	2.0 ± 1.0	NR
Wang et al. [70]	2013	USA	RS	RFA	94	CRLM	1.75	Tumor size, for each 5 mm increase (HR = 1.22, 95% CI: 1.02–1.49; p = .028)Ablative margin, for each 5 mm increase (HR = .54, 95% CI .36–.79; p = .002) Ablative margin, for each 5 mm increase (HR = 0.54, 95% CI 0.36–0.79; p = 0.002)
Ye et al. [71]	2018	China	PS	RFA	55 (55)	HCC	2.0 ± 0.7	NR
Yoon et al. [72]	2019	South Korea	PS	RFA	68 (88)	HCC	1.6 ± 0.6	Locally progressed tumor (OR = 8.67, 95% CI: 1.43–52.49; p = .019)Insufficient ablative margin (OR = 7.12, 95% CI: 1.49–34.12; p = .014) Insufficient ablative margin (OR = 7.12, 95% CI: 1.49–34.12; p = 0.014)
Zhang et al. [73]	2019	China	PS	RFA	84	HCC	2.1 ± 0.7	AM ≥5 mm on 3D-CEUS-FI (p = .024)
Zhong-Zhen et al. [74]	2013	China	PS	RFA	41 (49)	HCC	1.8 ± 0.86	NR

Figure 2. Risk of bias according to Newcastle-Ottawa Scale for selection, comparability, outcome and overall risk of bias.

Table 2. Ablative margin and measurement characteristics of studies investigating hepatocellular carcinoma. AM = ablative margin; LTP = local tumor progression; CT = computer tomography; CECT = contrast enhanced CT; MRI = magnetic resonance imaging; CEMRI = contrast enhanced MRI; US = ultrasound; CEUS = contrast enhanced US. *Results from rigid registered analysis is given; **Results from non-rigid registered analysis is given.

Reference	Pre-ablation imaging	Time from treatment	Post-ablation imaging	Time from treatment	Registration	AM method	Median follow-up	Ablation margins	Lesions/ patients	LTP rate
An et al. [33]	CEMRI	<1 month	CEMRI	<3 months	Non-rigid	2D	28.9 months	≤5 mm	61	26.2%
								>5 mm	80	3.8%
An et al. [34]	CEMRI	NR	CEMRI	<1 week	Rigid	3D	21 months	≤5 mm	24	50.0%
								>5 mm	44	9.1%
Du et al. [36]	CECT	NR	CECT	NR	Rigid	2D	30 months	5-8 mm	16	43.8%
								8-10 mm	16	6.3%
								≥10 mm	10	10.0%
Fukuda et al. [38]	CEMRI	<8 hours	CEMRI	4–7 days	Visual	2D	40 months	AM(-)	11
								AM(0)	24	34.0%
								AM(+)	50	2.0%
Hendriks et al. [39]	CECT	Intraprocedural	CECT	Intraprocedural	Non-rigid	2D	9.5 months	<0 mm	12	66.7%
								>0 mm	6	0.0%
Hocquelet et al. [40]	CEMRI	NR	CEMRI	1 month	Non-rigid	3D	26 months	976 ± 1064 mm^2 <5 mm	8	100.0%
								319 ± 385 mm^2 <5 mm	8	0.0%
Inoue et al. [41] *	CECT	<1 month	CEUS/CECT	1–3 days	Visual	2D	28.7 ± 14 months	<0	3
								0–5	49	18.0%
								>5	33	0.0%
Jiang et al. [43]	CECT	1 week	CECT	1 month	Rigid	3D	26 months	<5 mm	101	35.1%
								≥5 mm	58	4.1%
Ke et al. [46]	CECT	Intraprocedural	CECT	Intraprocedural	Visual	2D	38.2 months	5-10 mm	158	70.9%
								>10 mm	123	44.7%
Laimer et al. [49]	CECT	Intraprocedural	CECT	Intraprocedural	Rigid	2D	26.0 ± 10.3 months	<5 mm	110	9.1%
								>5 mm	66	0.0%
Kim et al. [47]	CT	NR	MRI	4–7 hours	Visual	2D	26.1 ± 5.7 months	AM(-)	1	40%
								AM(0)	9
								AM(+)	32	3.1%
Li et al. [50]	MRI	<1 month	MRI	<1 month	Rigid	2D	19.9 months	Continuous	444	44.0%
Li et al. [51]	CT/MRI	NR	CEUS	Intraprocedural	NR	2D	23 months	<5 mm	43	11.6%
								>5 mm	82	1.2%
Makino et al. [52]	CECT	NR	CECT	<7 days	Rigid	2D	21 months	<0 mm	23	44.6%
								0-5 mm	61	13.1%
								≥5 mm	10	0.0%
Makino et al. [53]	CT/MRI	<2 months	US	Intraprocedural	NR	2D	12 months	<0 mm	0
								0-5 mm	73	8.90%
								≥5 mm	6	0%
Matsuki et al. [54]	None	None	CECT/CEMRI	<7 hours	NR	2D	26.3 ± 12.7 months	AM(-)	6	50.0%
								AM(+)	42	4.8%
Minami et al. [55]	US/CECT/MRI	US: Intraprocedural CECT/MRI: NR	US/CECT/MRI	US: Intraprocedural CECT/MRI: NR	Visual	2D	19 months	<5 mm	253	5.5%
								>5 mm	321	0%
Park et al. [56]	MRI	NR	CECT	Immediate post-ablation	Non-rigid	2D	32 months	0-2 mm	34	32.4%
								2-5 mm	32	9.4%
								≥5 mm	112	2.7%
Sakakibara et al. [58]	CECT/CEMRI	NR	CECT/CEMRI	NR	Rigid	2D	NR	<0 mm	39	34.5%
								0 mm	41	12.5%
								5 mm	41	8.5%
								≥5 mm	12	0.0%
Sanga et al. [59]	CEUS	Intraprocedural	CEUS	Intraprocedural	Rigid	2D	21.4 months	Incomplete	1
								Grade C (0 mm)	0
								Grade B (0-5 mm)	25	4.0%
								Grade A (≥5 mm)	24	0.0%
Shin et al. [61]	CECT	<6 weeks	CECT	Intraprocedural	Non-rigid	2D	29.2 ± 10.8 months	<2 mm	14	14.3%
								≥2 mm	136	10.3%
Solbiati et al. [62]	CECT	NR	CECT	<1 day	Non-rigid	3D	12 months	100% >5 mm	24	0.0%
								90–99% >5 mm	17	5.9%
								50–89% >5 mm	30	16.7%
								0–49% >5 mm	2	100.0%
								Incomplete	17	76.5%
Takeyama et al. [64]	CEMRI	<3 months	CEMRI/MRI	<3 days	Rigid	2D	37.9 months	AM(+)	30	3.3%
								AM(0)	25	32.0%
								AM(-)	3	100.0%
Tang et al. [65]	CECT	NR	CECT	1 month	Rigid	3D		0-5 mm	39
								≥5 mm	36
Tokunaga et al. [66]	None	None	CEMRI	7 days	Visual	2D	20 ± 5 months	AM(+)	17	0.0%
								AM(0)	35	11.8%
								AM(-)	3
Toshikuni et al. [67]	CECT/MRI/CEUS	NR	US	Intraprocedural	Rigid	2D	27 months	incomplete	12%	8.3%
								Incomplete	40%	12.6%
Wang et al. [69]	CEMRI	NR	CEMRI	1 month	Rigid	2D	14.2 ± 5.4 months	0-5 mm	29	13.8%
								>5 mm	32	0.0%
Ye et al. [71]	3D-CEUS	Intraprocedural	3D-CEUS	Intraprocedural	Rigid	2D	13.6 months	<5 mm	28	28.0%
								≥5 mm	25	0.0%
Yoon et al. [72] **	CEMRI	<30 days	CECT	Immediate post-ablation	Non-rigid	2D	48 months	<3 mm	10	66.7%
								>3 mm	57	24.6%
Zhang et al. [73]	3D-CEUS	Intraprocedural	3D-CEUS	Intraprocedural	Rigid	2D	12.5 ± 4.8 months	<5 mm	49	16.3%
								≥5 mm	28	0.0%
ZhongZhen et al. [74]	CEMRI/CECT	NR	3D-CEUS	Intraprocedural	Rigid	2D	38 months	<5 mm	13	30.8%
								≥5 mm	27	0.0%

Figure 3. Forest plot and risk difference calculation for studies investigating HCC. LTP = local tumor progression; AM = ablative margin.

Table 3. Ablative margin and measurement characteristics of studies investigating colorectal liver metastases. AM = ablative margin; LTP = local tumor progression; CT = computer tomography; CECT = contrast enhanced CT; MRI = magnetic resonance imaging; CEMRI = contrast enhanced MRI. *Results from rigid registered analysis is given.

Reference	Pre-ablation imaging	Time from treatment	Post-ablation imaging	Time from treatment	Registration	AM method	Median follow-up	Ablation margins	Lesions/ patients	LTP rate
Faber et al. [37]	MRI/CECT	NR	CECT	Intraprocedural	Rigid	3D	24 months	Positive (2.4 ± 2.5 mm)	17
								Negative (−4.7 ± 2.7 mm)	12
								−6.6 mm median		0,0%
								0.5 mm median		100,0%
Izaaryene et al. [42]	MRI/CECT	<30 days	MRI	1 month	Visual	2D	13.3 months	<1 mm	5	100,0%
								2-5 mm	15	73,3%
								6-10 mm	12	8,3%
								>10 mm	7	0,0%
Kaye et al. [45]	CECT	NR	CECT/MRI/PET-CT	4–8 weeks	Rigid	3D	24 months	Incomplete	31	90,3%
								0 mm	6	100,0%
								1-5 mm	29	51,7%
								6-10 mm	21	4,8%
								>10 mm	6	0,0%
Laimer et al. [48]	CECT	Intraprocedural	CECT	Intraprocedural	Non-rigid	3D	36.1 ± 18.5 months	≥3 mm > 90%	74	9,4%
								≥3 mm > 95%	68	6,9%
								≥3 mm 100%	55	0,0%
Ruiter et al. [57]	CECT	Intraprocedural	CECT	Intraprocedural	NR	3D	1 year	−2.4 mm median	10	100,0%
								0.0 mm median	55	0,0%
Shady et al. [60]	CECT	NR	CECT	6 weeks	Visual	2D	RFA: 56 months MWA: 29 months	<5 mm	77	70.8%
								5-10 mm	46	13%
								>10 mm	22	0%
Sibinga Mulder et al. [27]	CECT	<2 months	CECT	Intraprocedural	Non-rigid	2D	44.7 ± 20.5 months	−2.6 mm average	9	100,0%
								2.1 mm average	9	0,0%
								Incomplete (≤0 mm)		88,9%
								Complete (≥1 mm)		11,1%
Vasiniotis Kamarinos et al. [68] *	CECT	Intraprocedural	CECT	Intraprocedural	Rigid	3D	21 months	<5 mm	74	50,0%
								>5 mm	30	10,0%
Wang et al. [70]	CECT	<6 weeks	CECT	4–8 weeks	Visual	2D	20 months	0 mm	30	74%
								1-5 mm	41	54%
								6-10 mm	15	26%
								11-15 mm	8	20%

Figure 4. Forest plot and risk difference calculation for studies investigating CRLM. LTP = local tumor progression; AM = ablative margin.

Table 4. Ablative margin and measurement characteristics of studies investigating mixed populations of HCC and CRLM. AM = ablative margin; LTP = local tumor progression; CT = computer tomography; CECT = contrast enhanced CT; MRI = magnetic resonance imaging; CEMRI = contrast enhanced MRI; CEUS = contrast enhanced ultrasound. * sufficient ablative margin is categorized as >5 mm for HCC, > 10 mm for CRLM.

Reference	Pre-ablation imaging	Time from treatment	Post-ablation imaging	Time from treatment	Registration	AM method	Median follow-up	Ablative margins	Lesions/ patients	LTP rate
Bo et al. [35]	CECT/CEMRI	NR	CEUS	1–3 days	Rigid	2D	2–34 months	<0 mm	4	25,0%
								0-5 mm	15	2,3%
								≥5 mm	28
Joo et al. [44] *	CT/MRI	<2 months	MRI	1 week	NR	2D	11 months	Insufficient	66	33,8%
								Sufficient	205	6,90%
Sparchez et al. [63]	CEUS	NR	CEUS	4 weeks	Rigid	2D	NR	≤5 mm	13	76,9%
								>5 mm	69	18,8%

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