Effects of energy-based ablation on thyroid function in treating benign thyroid nodules: a systematic review and meta-analysis

Figures & data

Figure 1. Study flow diagram.

Table 1 Characteristics of included studies

Study	Year published	Sampling year	Country	Center	Design	No. participants	Age(years) Mean ± SD(range)	Sex(F/M)	Intervention	Follow-up (months)	Outcomes	NOS score
Papini et al.[51]	2004	2002.4-2002.11	Italy	Ospedale Regina Apostolorum	prospective	20	63.3 ± 14.1(30-80)	15/5	LA	6	TSH,FT3,FT4,TPOAb	8
Cakir et al. [50]	2006	N.A.	Turkey	Bilkent	prospective	12	47.42 ± 17.1(20-78)	8/4	LA	12	TSH,FT3,FT4,TPOAb,TgAb	7
Papini et al. [49]	2007	2003.1-2004.4	Italy	Ospedale Regina Apostolorum	prospective	21	44.9 ± 5.1	18/3	LA	12	TSH,FT3,FT4,TPOAb,TgAb	8
Maurilio et al. [48]	2008	2004.4-2005.12	Italy	“Federico II” University of Naples	prospective	9	66.8 ± 12.1	6/3	RFA	≥6	TSH,FT4	6
Baek et al. [47]	2009	2007.1-2007.9	Korea	Daerim St. Mary’s Hospital	prospective	15	40.87 ± 11.1(29-66)	12/3	RFA	6-8	TSH,FT3,FT4	7
Roberto et al. [46]	2010	2004.1-2006.12	Italy	Arcispedale Santa Maria Nuova	retrospective	122	52.2 ± 12.3(20-83)	95/27	LA	36	TSH,FT3,FT4,Tg	7
Feng et al. [45]	2012	2010.11-2011.8	China	Chinese People’s Liberation Army General Hospital	prospective	11	50 ± 7(39-59)	10/1	MWA(cooled)	1-9	TSH,T3,FT4	6
Døssing et al. [44]	2013	N.A.	Denmark	Odense University Hospital	prospective	22	49(39-56)	17/5	LA	6	TSH, TPOAb	8
Giovanni et al. [43]	2012	2005-2008	Italy	University of Perugia	retrospective	20	62(53-72)	N.A.	LA	36	TSH,FT4	6
Giovanni* et al. [43]	2012	2005-2008	Italy	University of Perugia	retrospective	20	64(55-73)	N.A.	LA	36	TSH,FT4	6
Cesareo et al. [42]	2014	2011.3-2013.9	Italy	“S.M.Goretti” Hospital	prospective	42	56 ± 14(24-80)	27/15	RFA	6	TSH,FT3,FT4	8
Kristina et al. [9]	2015	2013.1-2014.7	Germany	University Hospital, Frankfurt am Main	prospective	30	54(32-79)	15/15	MWA(uncooled)	6	TSH,T3,T4,TgAb,TPOAb	6
Hong et al. [8]	2014	2007.1-2012.10	Korea	University of Ulsan College of Medicine	retrospective	18	49.9(27-81)	16/2	RFA	6	TSH,FT4,T3	6
Korkusuz et al. [7]	2015	N.A.	Germany	University Hospital, Frankfurt am Main	retrospective	12	56.9(37-81)	9/3	HIFU	3	TSH,T3,T4,TgAb,TPOAb	6
Pacella et al. [41]	2015	2004.1-2013.12	Italy	Regina Apostolorum Hospital	retrospective	1531	54.1	1087/444	LA	12	TSH,FT4	6
Valcavi et al. [12]	2015	2012.1-2014.2	Italy	Arcispedale Santa Maria Nuova and Clinica Cancer Research Institute	prospective	40	54.9 ± 14.3(18-84)	35/5	RFA	24	TSH,FT4,FT3	6
Li et al. [40]	2016	2013.4-2015.3	China	Shanghai Tenth People’s Hospital	prospective	35	42.7 ± 14.9(17-67)	27/8	RFA	6	TSH,FT4,FT3	8
Negro et al. [39]	2016	2009.7-2012.3	Italy	“V. Fazzi” Hospital	retrospective	56	54.7 ± 11.7	42/14	LA	48	TSH,FT4,FT3	6
Cesareo et al. [11]	2017	2012.6-2015.11	Italy	“S. M. Goretti” Hospital	retrospective	48	57.7 ± 14(24-80)	31/17	RFA	12	TSH,FT4,FT3	6
Kim et al. [37]	2016	2009.10-2015.5	Korea	University of Ulsan College of Medicine	retrospective	746	48.3 ± 13.9	648/98	RFA	12	Description of thyroid disorders	6
Lang et al. [36]	2017	2015.8-2016.4	China	The University of Hong Kong	retrospective	43	47.9 ± 11.8	41/2	HIFU	6	TSH,FT4	6
Lang@ et al. [35]	2017	2015.8-2016.12	China	The University of Hong Kong	retrospective	76	50.9 ± 11.5	64/12	HIFU	6	Description of thyroid disorders	6
Liu et al. [34]	2017	2012.9-2015.8	China	Capital Medical University	retrospective	435	49.9 ± 0.9(24-76)	309/126	MWA(cooled)	>12	TSH,T3,T4	6
Pacella et al. [33]	2017	2009.5-2014.12	Italy	“Regina Apostolorum” Hospital	retrospective	449	57 ± 14	69/31	LA	>12	Description of thyroid disorders	6
Pacella* et al. [33]	2017	2009.5-2014.12	Italy	“Regina Apostolorum” Hospital	retrospective	152	57 ± 14	76/24	RFA	>12	Description of thyroid disorders	6
Wang et al. [32]	2017	2013.1-2015.1	China	Chinese PLA General Hospital	retrospective	110	N.A.	98/12	MWA(cooled)	>12	TSH,FT4,FT3	6
Wu et al. [31]	2017	2014.8-2015.12	China	The First Affiliated Hospital of Soochow University	retrospective	100	42 ± 11.6(19-66)	72/28	MWA(cooled)	12	TSH,FT4,FT3,TgAb,TPOAb	6
Jung et al. [30]	2018	2010.5-2011.12	Korea	University of Ulsan College of Medicine	prospective	276	46.3 ± 12.8(15-79)	244/32	RFA	>12	Description of thyroid disorders	6
Lang et al. [29]	2018	2015.11-2017.12	China	The University of Hong Kong	retrospective	85	43.19 ± 11.5	76/9	HIFU	6	TSH,FT4,TgAb	7
Lang* et al. [29]	2018	2015.11-2017.12	China	The University of Hong Kong	retrospective	191	49.37 ± 11.6	159/32	HIFU	6	TSH,FT4,TgAb	7
Oddo et al. [28]	2017	2014.9-2015.9	Italy	IRCSS San Martino University Hospital-IST	prospective	14	55 ± 10(38-72)	12/2	LA	12	TSH,FT3,FT4,TPOAb,TgAb	6
Antonio et al. [27]	2018	2011.1-2012.10	Italy	Hospital Israelita Albert Einstein	prospective	30	46.06(18-84)	29/1	LA	12	TSH,FT4,TgAb,TPOAb	6
Wei et al. [26]	2018	2013.10-2017.2	China	Beijing Friendship Hospital	retrospective	230	50.5 ± 13(14-82)	163/67	MWA(cooled)	>12	TSH,T3,T4	6
Tang et al. [25]	2018	2015.10-2016.7	China	Renji Hospital	retrospective	194	50(17-83)	157/37	RFA	1	TSH,FT3,FT4,TgAb,TPOAb	8
Tang* et al. [25]	2018	2016.8-2017.5	China	Renji Hospital	retrospective	188	48(25-79)	144/44	RFA	1	TSH,FT3,FT4,TgAb,TPOAb	8
Hamou et al. [24]	2018	2013.10-2017.11	France	CHU Lille	retrospective	99	49.7 ± 12.2	80/19	RFA	18	Description of thyroid disorders	6
Hamou* et al. [24]	2018	2013.10-2017.11	France	CHU Lille	retrospective	67	54.8 ± 12.4	53/14	LA	18	Description of thyroid disorders	6
Cappelli et al. [23]	2019	2017.8-2018.5	Italy	University of Brescia	retrospective	26	49.3 ± 17.1	19/7	RFA	12	TSH,FT4	6
de Freitas et al. [22]	2019	N.A.	Brazil	Instituto do Cancer do Estado de Sao Paulo Octavio Frias de Oliveira	prospective	21	56.2 ± 12	20/1	LA	12	TSH,FT4,T3,TgAb,TPOAb	8
Lang@ et al. [21]	2018	2015-2017.6	China	The University of Hong Kong	retrospective	77	49 ± 13	65/12	HIFU	>6	Description of thyroid disorders	6
Lang et al. [20]	2019	2015.8-2018.5	China	The University of Hong Kong	retrospective	31	50.87 ± 9.84	22/9	HIFU	>6	TSH,FT4,TgAb,TPOAb	6
Lang * et al. [20]	2019	2015.8-2018.5	China	The University of Hong Kong	retrospective	19	52.89 ± 16.2	15/4	HIFU	>6	TSH,FT4,TgAb,TPOAb	6
Liu et al. [19]	2019	2016.2-2017.8	China	Jiaozuo Second People’s Hospital	retrospective	72	44.4 ± 9.6	46/26	MWA(cooled)	>6	TSH,FT4,FT3	8
Negro et al. [18]	2019	2009.7-2012.3	Italy	“V. Fazzi” Hospital	retrospective	62	54.7 ± 11.7	47/15	LA	60	TgAb,TPOAb	6
Rabuffi et al. [17]	2019	2013.5-2016.6	Italy	San Giovanni Addolorata Hospital	retrospective	77	57.5 ± 15.5(30-75)	55/22	RFA	12	TSH,FT4,FT3,TgAb.TPOAb	6
Cesareo et al. [16]	2019	2016.1-2018.11	Italy	S. M. Goretti Hospital	prospective	30	59.3 ± 11.7	N.A.	LA	6	TSH,TgAb,TPOAb	6
Cesareo* et al. [16]	2019	2016.1-2018.11	Italy	S. M. Goretti Hospital	prospective	30	53.3 ± 14.3	N.A.	RFA	6	TSH,TgAb,TPOAb	6
Zhu et al. [15]	2019	2017.6-2018.5	China	Chinese PLA General Hospital	retrospective	76	46 ± 14	44/32	RFA	>6	TSH,FT4,FT3,TgAb,TPOAb	7
Zhu* et al. [15]	2019	2017.6-2018.5	China	Chinese PLA General Hospital	retrospective	290	49 ± 14	191/99	RFA	>6	TSH,FT4,FT3,TgAb,TPOAb	7

NOS, Newcastle-Ottawa quality assessment scale; N.A., not applicable; No., number;

*The second arm of one study. @the second article published by same author within one year.

Figure 2. Forest plots demonstrating changes in TSH of various follow-up period.

Figure 3. Forest plots demonstrating changes in FT4 of various follow-up period.

Figure 4. Forest plots demonstrating changes in FT3 of various follow-up period.

Table 2. New onset of thyroid abnormalities.

Number	1 Month	3 Months	6 Months	12 Months	2 Years	3 Years
Studies	9	4	14	4	1	1
Euthyroidism	1210	245	1961	329	112	119
Hypothyroidism (%)	2 (0.16)	1 (0.41)^a	5 (0.25)	0	0	0
Hyperthyroidism (%)	5 (0.41)	0 (0)	4 (0.20)	0	0	0

^aThe patient was subclinical hypothyroidism.

Table 3. Sensitivity analysis.

Index	Study omitted		95% CI	Log-rank p value	I^2	p Value
		MD
6-month TSH	Liu 2017	0.13	0.01 to 0.26	0.007	51	0.04
12-month FT4	Roberto 2010	0.42	0.09 to 0.75	0.19	25	0.01
		SMD
3-month Tg	Cakir 2006	−0.20	−0.39 to -0.01	0.86	0	0.04
3-month TgAb	Zhu 2019	0.18	0.04 to 0.33	0.78	0	0.01
3-month TPOAb	Zhu 2019	0.22	0.08 to 0.37	0.82	0	0.002
6-month TPOAb	Zhu 2019	0.17	0.01 to 0.34	0.33	14	0.04

MD: mean difference; SMD: standard mean difference; CI: confidence interval.

Table 4. Subgroup analysis of TSH level.

TSH	No. of studies	MD (95% CI)	Log-rank p value	I^2 (%)	p Value
1m postablation	15	−0.06 [−0.14 to 0.02]	0.66	0	0.16
Country
China	8	−0.07 [−0.17 to 0.02]	0.25	22	0.14
Non-China	7	−0.02 [−0.19 to 0.15]	0.91	0	0.81
Study design
Retrospective	9	−0.08 [−0.17 to 0.02]	0.42	1	0.10
Prospective	6	0.00 [−0.17 to 0.18]	0.76	0	0.96
Intervention
LA	4	0.01 [−0.19 to 0.21]	0.64	0	0.93
RFA	8	−0.07 [−0.20 to 0.07]	0.91	0	0.31
MWA	3	−0.08 [−0.37 to 0.21]	0.04	69	0.60
HIFU	0
Sample size
<100	8	−0.00 [−0.18 to 0.17]	0.91	0	0.99
≥100	7	−0.08 [−0.17 to 0.02]	0.23	26	0.11
6m postablation	19	0.07 [−0.09 to 0.23]	<0.00001	72	0.39
Country
China	5	−0.13 [−0.52 to 0.25]	<0.00001	84	0.49
Non-China	14	0.15 [−0.02 to 0.31]	0.002	60	0.08
Study type
Retrospective	9	−0.01 [−0.26 to 0.23]	<0.00001	80	0.91
Prospective	10	0.15 [−0.07 to 0.38]	0.004	63	0.19
Intervention
LA	8	0.16 [−0.11 to 0.43]	0.0007	72	0.25
RFA	7	0.18 [0.06 to 0.30]	0.30	17	0.002*
MWA	4	−0.13 [−0.60 to 0.33]	<0.0001	88	0.58
HIFU	0
Sample size
<100	15	0.13 [−0.03 to 0.28]	0.002	58	0.12
≥100	4	−0.11 [−0.55 to 0.32]	<0.0001	89	0.61
12m postablation	17	0.10 [−0.06 to −0.14]	0.72	0	<0.0001*
Country
China	4	−0.01 [−0.23 to 0.20]	0.41	0	0.91
Non-China	13	0.10 [0.06 to 0.15]	0.76	0	<0.00001*
Study type
Retrospective	11	0.10 [0.06 to 0.15]	0.84	0	<0.0001*
Prospective	6	0.07 [−0.11 to 0.26]	0.26	24	0.44
Intervention
LA	10	0.10 [0.06 to 0.15]	0.57	0	<0.0001*
RFA	4	0.14 [−0.01 to 0.30]	0.83	0	0.07
MWA	3	−0.06 [−0.30 to 0.17]	0.45	0	0.59
HIFU	0
Sample size
<100	12	0.12 [0.01.0.23]	0.69	0	0.04*
≥100	5	0.10 [0.05 to 0.14]	0.41	0	<0.0001*

MD: mean difference; CI: confidence interval.

*p<0.05 in the subgroup analysis.

Table 5. Subgroup analysis of FT3 level.

FT3	No. of studies	MD (95%CI)	Log-rank p value	I^2 (%)	p Value
1m postablation	10	−0.05 [−0.30 to 0.20]	<0.00001	89	0.72
Country
China	5	0.16 [−0.27 to 0.59]	<0.00001	92	0.46
Non-China	5	−0.19 [−0.55 to 0.17]	<0.00001	87	0.30
Study design
Retrospective	6	0.11 [−0.23 to 0.45]	<0.00001	91	0.52
Prospective	4	−0.25 [−0.68 to 0.19]	0.00001	86	0.27
Intervention
LA	3	0.03 [−0.14 to 0.20]	0.76	0	0.77
RFA	6	−0.31 [−0.53 to −0.08]	<0.00001	83	0.008*
MWA	1
HIFU	0
Sample size
<100	5	−0.21 [−0.54 to 0.11]	<0.00001	86	0.19
≥100	5	0.22 [−0.29 to 0.72]	<0.00001	93	0.40
6m postablation	10	0.06 [−0.17 to 0.29]	<0.00001	86	0.62
Country
China	4	0.23 [−0.22 to 0.67]	<0.00001	94	0.31
Non-China	6	−0.05 [−0.23 to 0.13]	0.10	46	0.48
Study type
Retrospective	6	0.15 [−0.13 to 0.43]	<0.00001	91	0.31
Prospective	4	−0.13 [−0.32 to 0.05]	0.21	34	0.16
Intervention
LA	5	−0.03 [−0.16 to 0.10]	0.06	56	0.66
RFA	3	−0.11 [−0.20 to −0.02]	0.0004	87	0.02*
MWA	2	0.13 [−0.12 to 0.38]	<0.00001	97	0.31
HIFU	0
Sample size
<100	7	−0.03 [−0.22 to 0.15]	0.03	58	0.72
≥100	3	0.31 [−0.23 to 0.84]	<0.00001	95	0.26
12m postablation	8	0.05 [−0.18 to 0.29]	0.001	70	0.65
Country
China	2	0.76 [−0.64 to 2.17]	<0.0001	93	0.28
Non-China	6	−0.08 [−0.21 to 0.05]	0.96	0	0.21
Study type
Retrospective	4	0.27 [−0.16 to 0.70]	0.001	85	0.22
Prospective	4	−0.13 [−0.31 to 0.06]	0.92	0	0.17
Intervention
LA	5	−0.06 [−0.21 to 0.09]	0.93	0	0.42
RFA	1
MWA	2	0.76 [−0.64 to 2.17]	<0.0001	93	0.28
HIFU	0
Sample size
<100	5	−0.11 [−0.27 to 0.05]	0.96	0	0.17
≥100	3	0.10 [−0.07 to 0.26]	<0.0001	90	0.24

MD: mean difference; CI: confidence interval.

*p<0.05 in the subgroup analysis.

Table 6. Subgroup analysis of FT4 level.

FT4	No. of studies	MD (95%CI)	Log-rank p value	I^2 (%)	p Value
1m postablation	13	−0.46 [−0.76 to −0.15]	0.28	16	0.004*
Country
China	6	−0.75 [−1.40 to −0.11]	0.05	54	0.02*
Non-China	7	−0.03 [−0.68 to 0.62]	0.97	0	0.92
Study design
Retrospective	7	−0.31 [−0.68 to 0.06]	0.98	0	0.10
Prospective	6	−0.64 [−1.60 to 0.31]	0.05	55	0.18
Intervention
LA	4	−0.05 [−0.90 to 0.79]	0.82	0	0.91
RFA	8	−0.52 [−0.87 to −0.16]	0.09	44	0.004*
MWA	1
HIFU	0
Sample size
<100	8	−0.71 [−1.19 to −0.23]	0.11	40	0.004*
≥100	5	−0.28 [−0.68 to 0.12]	0.94	0	0.17
6m postablation	16	−0.14 [−0.40 to 0.12]	0.83	0	0.29
Country
China	12	−0.29 [−0.67 to 0.08]	0.77	0	0.13
Non-China	4	−0.00 [−0.36 to 0.35]	0.73	0	0.99
Study type
Retrospective	8	−0.11 [−0.41 to 0.18]	0.51	0	0.45
Prospective	8	−0.21 [−0.73 to 0.30]	0.84	0	0.42
Intervention
LA	7	−0.37 [−0.82 to 0.07]	0.45	0	0.10
RFA	7	−0.08 [−0.41 to 0.26]	0.98	0	0.66
MWA	2	0.45 [−0.53 to 1.44]	0.55	0	0.37
HIFU	0
Sample size
<100	13	−0.11 [−0.49 to 0.28]	0.98	0	0.59
≥100	3	−0.20 [−0.96 to 0.56]	0.05	66	0.61
12m postablation	15	0.20 [−0.30 to 0.71]	0.004	56	0.43
Country
China	3	0.87 [0.25 to 1.49]	0.41	0	0.006*
Non-China	12	0.07 [−0.50 to 0.64]	0.01	54	0.81
Study type
Retrospective	9	0.17 [−0.57 to 0.91]	0.001	69	0.65
Prospective	6	0.22 [−0.31 to 0.76]	0.30	18	0.42
Intervention
LA	9	−0.38 [−0.79 to 0.02]	0.25	21	0.07
RFA	4	1.05 [0.33 to 1.77]	0.56	0	0.004*
MWA	2	0.95 [0.30 to 1.60]	0.29	11	0.004*
HIFU	0
Sample size
<100	12	0.24 [−0.19 to 0.67]	0.31	13	0.24
≥100	3	0.06 [−1.59 to 1.71]	<0.0001	89	0.94

MD: mean difference; CI: confidence interval.

*p<0.05 in the subgroup analysis.

Figure 5. (A) Funnel plot detailing publication bias in the studies reporting changes of TSH level at 1st, 3rd and 12th month after ablation therapy. (B) Funnel plot detailing publication bias in the studies reporting changes of FT4 level at 1st, 6th and 12th month after ablation therapy.

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Data availability statement

The data collected to support the findings of this study are included within the article.