https://orcid.org/0000-0002-3298-3705
Abstract
Purpose
To analyze the outcomes of radiofrequency ablation (RFA) for isthmus papillary thyroid cancer (PTC) versus PTC originating from the lobes.
Methods
Patients with solitary low-risk PTC treated with RFA between July 2014 and December 2019 were retrospectively reviewed. This study was approved by our institutional review board. Of the 562 patients, 104 and 458 had PTCs located in the thyroid isthmus and thyroid lobes, respectively. Local tumor progression (LTP), LTP-free survival (LTPFS), changes in tumor volume, and complications were compared between the two groups using propensity-score matching (PSM).
Results
The isthmic and lobar groups showed no significant differences in LTP (2.9% vs. 3.8%), new PTC (2.9% vs. 2.9%), persistent lesions (0.0% vs. 0.2%), or LTPFS after PSM. Before PSM, the two groups showed significant differences in the volume reduction ratio (VRR) of the ablated tumors at 1, 3, 24, 30, and 48 months after RFA, but no differences between the two groups were observed in tumor volume, VRR, or disappearance rate after PSM (p > .05). One patient in the isthmic group presented with coughing, while another complained of hoarseness. Complications did not differ significantly between the two groups (p > .05).
Conclusions
The outcomes of RFA for patients with low-risk PTC in the thyroid isthmus and thyroid lobes were similar. Therefore, RFA may serve as an alternative treatment option for patients with low-risk isthmic PTC.
1. Introduction
Papillary thyroid cancer (PTC) is the most frequent subtype of differentiated thyroid cancer, accounting for 80–85% of all thyroid cancers [Citation1]. The incidence of PTC, especially papillary thyroid microcarcinoma (PTMC), has increased sharply over the past few decades [Citation2,Citation3]. Isthmic PTC is defined as a thyroid cancer in which the tumor center is located between two lines perpendicular to the surface of the skin from the most lateral points of the trachea [Citation4]. Previous studies have reported that the incidence of isthmic PTC ranges from 1% to 9.2% [Citation5–7]. To date, no specific guidelines have been proposed for the management of isthmic PTC. Some studies suggest that isthmic PTC is more likely to show more aggressive behavior, such as more frequent lymph node metastasis (LNM), multifocality, and capsular invasion, than PTC located in the thyroid lobes [Citation8–10]; therefore, some surgeons prefer total thyroidectomy and prophylactic central compartment lymph node dissection. However, complications related to total thyroidectomy, including hypothyroidism requiring lifelong administration of levothyroxine, permanent recurrent laryngeal nerve (RLN) injury, and inadvertent hypoparathyroidism [Citation11], have considerable effects on patients’ quality of life.
Ultrasonography (US)-guided thermal ablation, including radiofrequency ablation (RFA), laser ablation, and microwave ablation, is an alternative to surgery in selected patients with low-risk PTC, and has yielded promising results [Citation12–16]. These findings are primarily based on cases of PTC arising in the thyroid lobes. Although several studies have addressed the efficacy and safety of thermal ablation for isthmic PTC [Citation4,Citation17,Citation18], to the best of our knowledge, no study has compared the outcomes of RFA in the treatment of low-risk PTC arising in the thyroid isthmus and bilateral lobes. Therefore, this study aimed to analyze the outcomes of RFA for isthmic PTC and evaluate whether the outcomes for these tumors differed from those for tumors originating in the thyroid lobes.
2. Materials and methods
2.1. Patients
This retrospective study was approved by the ethics committee of our hospital (S2019-211-01), which waived the requirement for informed consent to do the research. Data from patients with low-risk PTC who underwent RFA between July 2014 and December 2019 were retrospectively collected. All patients provided written informed consent before RFA at our hospital, and before seeking consent, the patients were explained that surgery is the standard treatment for PTC, and that RFA cannot eliminate occult PTC and cervical LNM. The inclusion criteria were as follows [Citation1]: core needle biopsy (CNB)-confirmed PTC [Citation2]; solitary PTC without an aggressive subtype, evidence of extrathyroidal extension, LNM, or distant metastasis [Citation3]; PTC with maximal diameter of > 0.5 cm and ≤ 2 cm on US [Citation4]; at least 12 months of follow-up; and [Citation5] ineligibility for or refusal to undergo surgery. The exclusion criteria were as follows [Citation1]: a history of neck irradiation [Citation2]; the presence of other malignant diseases [Citation3]; age ≤ 18 years; and [Citation4] breastfeeding or pregnancy. Patients were divided into two groups according to the PTC location: an isthmic group (PTC originating from the thyroid isthmus) and a lobar group (PTC originating from the thyroid bilateral lobes).
2.2. Pre-ablation assessment
All patients underwent thyroid US (S2000; Siemens, Mountain View, CA; Sequoia 512, Siemens, Mountain View, CA; Mylab Twice II, Esaote, Genoa, Italy; Resona 7, Mindray, Shenzhen, China) using a 5–12-MHz linear array probe before RFA. Three orthogonal tumor dimensions were measured, and the volume was calculated using the following equation: volume = length × width × depth × 0.524 [Citation19]. US features (composition, echogenicity, shape, margin, and calcification) were recorded according to the American College of Radiology Thyroid Imaging Reporting and Data System [Citation20]. The tumor location was categorized as the thyroid lobe or isthmus.
Laboratory tests, including complete blood count, blood coagulation battery, and thyroid function tests, were performed before RFA. Neck and chest computed tomography (CT) were recommended to perform in order to exclude metastases.
2.3. Ablation procedure
RFA procedures were performed by experienced US physicians with more than 10 years of experience in thyroid imaging and interventional US. A bipolar radiofrequency ablation system (CelonLab POWER, Hamburg, Germany) was used in this study. Depending on the size and location of the targeted tumor, an 18-G electrode with a 0.9- or 1.5-cm active tip and a 10-cm shaft length were applied (Celon ProSurge Micro 100-T09 or 100-T15; Hamburg, Germany).
Patients were placed in the supine position with their necks extended. Local anesthesia was administered using 1% lidocaine after routine skin sterilization. The hydrodissection technique was used to protect vital organs (i.e., the RLN, common carotid artery, jugular vein, trachea, and esophagus) from thermal injuries [Citation21]. The trans-isthmic approach and moving-shot technique were used during RFA [Citation22]. The output power was 3–9 W. The ablation was terminated after hyperechogenicity covered the entire tumor and the ablation zone extended at least 3 mm beyond the tumor margins to prevent marginal recurrence [Citation23]. The ablation area was evaluated with contrast-enhanced ultrasound. If an enhanced area within the tumor was observed or the extension beyond the tumor margin was insufficient, complementary ablation was performed. Patients were closely observed for 1–2 h before discharge.
2.4. Post-ablation evaluation and follow-up
The patients underwent follow-up assessments at 1, 3, 6, and 12 months post-ablation and every 6–12 months thereafter. US and thyroid function tests were performed at each follow-up examination. The volume reduction ratio (VRR) was calculated with the following equation: VRR = ([initial volume − final volume] × 100)/initial volume [Citation24]. At 3 or 6 months post-ablation, CNB was recommended for the central and peripheral zones as well as the surrounding thyroid parenchyma of the ablation zone. New malignant tumors or suspected metastatic lymph nodes were confirmed by CNB. Additional ablation or surgery was performed for new PTCs or metastatic lymph nodes based on patient preference. Neck and chest CT scans were performed annually post-ablation to rule out metastases. Positron emission tomography or a bone scan was performed if symptoms indicative of distant metastases were noted. Patients did not take levothyroxine if their serum thyroid-stimulating hormone (TSH) levels remained between 0.5 and 2 mU/L without medication after RFA. Some patients who received thyroid hormone supplementation after RFA gradually tapered their dosage or stopped it completely if their serum TSH levels improved and the ablated tumor disappeared during the follow-up period.
2.5. Study endpoints and definitions
The primary endpoints were local tumor progression (LTP) and LTP-free survival (LTPFS). LTP was confirmed by biopsy, and classified into new malignant tumors, persistent lesions, or cervical LNM [Citation23]. LTPFS was defined as the interval from the initial RFA to LTP or the last follow-up. Because distant metastasis was not found in this study, it was not considered.
The secondary endpoints were changes in the ablated zone volume and complications. Complications were classified according to the standards of the Society of Interventional Radiology [Citation25]. Occurrences that were sometimes inevitable, such as tolerable mild pain/discomfort not requiring medication, and a minimal amount of bleeding/parenchymal edema without induction of symptoms, were not regarded as complications or adverse effects [Citation26].
2.6. Statistical analysis
The Kolmogorov–Smirnov test was used to assess the distribution of continuous data, and the homogeneity of variances was assessed using the Levene test. Normally distributed continuous data were presented as means ± standard deviations and compared using an independent-sample t test. Non-normally distributed continuous variables were expressed as medians and interquartile ranges and compared using the Mann–Whitney U test. Categorical data were expressed as frequencies and percentages. The χ2 or Fisher’s exact test was performed to compare categorical data wherever appropriate. LTPFS curves were estimated using the Kaplan–Meier method, and the log-rank test was used to compare differences. Propensity-score matching (PSM) was used to reduce selection bias and confounding differences. Patient age, sex, follow-up period, maximal tumor diameter and volume, and US characteristics were matched using 1:1 nearest-neighbor matching [Citation27].
Statistical analyses were performed using SPSS for Windows (version 21.0; IBM Corp., Armonk, NY, USA) and R software (version 4.2.1; MatchIt packages). Differences were considered statistically significant at p < .05.
3. Results
3.1. Baseline characteristics before PSM
Among the 3782 patients who underwent RFA for thyroid nodules at our institution between July 2014 and December 2019, 562 met the inclusion criteria before PSM (). Of these, 104 patients (18.5%) had tumors in the thyroid isthmus, while 458 (81.5%) showed tumors in the thyroid lobes. Among these 562 patients, 97 (17.3%) were ineligible for surgery because of the high risk associated with general anesthesia, while 465 (82.7%) refused surgery for cosmetic reasons or concerns about surgery-related complications. The patients in the isthmic group were older than those in the lobar group (p < .05). In terms of shape, isthmic PTCs were wider than lobar PTCs (p < .05). The margins of the isthmic PTCs were smooth or ill-defined, whereas those of the lobar PTCs were irregular or lobulated (p < .05). The two groups showed no statistically significant differences in sex, maximal tumor diameter, or follow-up period (p > .05).
Table 1. Baseline characteristics of patients with low-risk PTC according to tumor location.
3.2. Clinical outcomes before PSM
The overall incidences of LTP, LNM, new PTC, and persistent lesions were 3.9% (22/562), 1.1% (6/562), 2.0% (11/562), and 0.9% (5/562), respectively. The isthmic and lobar groups showed no significant differences in the incidences of LTP (2.9% vs. 4.1%, p = .780), LNM (0.0% vs. 1.3%, p = .599), new PTC (2.9% vs. 1.7%, p = .436), or persistent lesions (0.0% vs. 1.1%, p = .590) (). In the isthmic group, three patients (2.9%) showed new PTC in the thyroid lobes after a mean follow-up period of 28.6 months (range, 12–84 months). All three patients underwent additional RFA successfully. In the lobar group, six patients (1.3%) developed LNM, and new PTC was found in eight patients (1.7%; five in the ipsilateral lobe and three in the contralateral lobe) after a mean follow-up period of 27.2 months (range, 12–72 months). Among the patients who developed LNM, five underwent RFA for metastatic lymph nodes and one underwent active surveillance (AS) in accordance with the patient’s preference. Among the patients with new PTC, seven underwent additional RFA and one underwent total thyroidectomy. A total of 287 patients underwent post-ablation CNB. Five patients (1.1%) had persistent lesions and underwent additional RFA. The two groups showed no significant differences in LTPFS ().
Figure 1. Kaplan–Meier analysis of local tumor progression-free survival in the isthmic and lobar groups before (A) and after (B) propensity-score matching.
Table 2. Comparison of local tumor progression between the two groups.
Owing to the expanded ablation, the ablated tumor volume at 1–3 months after RFA was larger than that before ablation and then decreased gradually ( and ). The two groups showed considerable differences in ablated tumor volume at 1, 3, 6, 24, 30, and 48 months after RFA (p < .05; Supplemental Table 1). The VRR at 1–3 months post-ablation was negative due to expanded ablation, and changed to positive at 6 months. The VRRs of ablated isthmic PTCs were larger than those of lobar PTCs at 1, 3, 24, 30, and 48 months after RFA (p < .05; Supplemental Table 2). At the 72-month follow-up visit, the VRR in both groups was 100%. During the follow-up period, 84 tumors (80.8%) disappeared in the isthmic group, and 334 tumors (72.9%) disappeared in the lobar group. The median disappearance time was 12 months in both groups. The two groups showed no significant differences in the disappearance rate and time (p > .05).
Figure 2. Imaging findings in a 46-year-old Man with papillary thyroid cancer treated with radiofrequency ablation. The tumor located in the thyroid isthmus with a volume of 1.17 cm3 (arrow) is shown in the longitudinal (A) and transverse (B) planes on ultrasonography. The tumor volume decreased to 0.76 cm3 (arrow, C), 0.26 cm3 (arrow, D), and 0.17 cm3 (arrow, E), respectively, at 1, 3, and 9 months after radiofrequency ablation and disappeared at 18 months (arrow, F).
Figure 3. Imaging findings in a 30-year-old Woman with papillary thyroid cancer treated with radiofrequency ablation. The tumor located in the left lobe of the thyroid with a volume of 0.88 cm3 (arrow) is shown in the longitudinal (A) and transverse (B) planes on ultrasonography. The tumor volume decreased to 0.63 cm3 (arrow, C), 0.47 cm3 (arrow, D), and 0.33 cm3 (arrow, E), respectively, at 1, 3, and 6 months after radiofrequency ablation, and only the needle track was visible at 12 months (arrow, F).
3.3. Baseline characteristics and clinical outcomes after PSM
After 1:1 PSM, the baseline characteristics of the 104 patients in each group were similar (). The overall incidences of LTP, new PTC, and persistent lesions were 3.4% (7/208), 2.9% (6/208), and 0.5% (1/208), respectively. New tumors accounted for most of the LTP cases. After a mean follow-up period of 28.6 months, three patients (2.9%) in the isthmic group and four (3.8%) in the lobar group showed LTP (). No significant differences were observed in the incidence of LTP (2.9% vs. 3.8%, p = 1.000), new PTC (2.9% vs. 2.9%, p = 1.000), or persistent lesions (0.0% vs. 0.2%, p = 1.000) between the two groups (). In the isthmus group, new PTC was found in the thyroid lobes of three patients (2.9%). The median interval between the initial RFA and LTP detection was 25 months. In the lobar group, new PTC was found in three patients (2.9%) and persistent lesion in one patient (1.1%). The median interval between the initial RFA and LTP detection was 26.5 months. Kaplan–Meier survival curves revealed no significant differences in LTPFS rates between the two groups ().
During follow-up, no difference was observed between the two groups in terms of the volume and VRR of the ablated tumor. A total of 84 tumors (80.8%) disappeared in the isthmic group, and 80 tumors (76.9%) disappeared in the lobar group. The median disappearance time was 12 months in the two groups. The two groups showed no significant differences in the disappearance rate and time (p > .05).
3.4. Complications
All the patients tolerated the RFA procedure well. After PSM, in the isthmic group, one patient (1.0%, 1/104) presented with coughing after RFA, which was relieved within one week. In the lobar group, one patient (1.0%, 1/104) complained of hoarseness and recovered within one month. No significant difference was found between the two groups in terms of complications (p > .05). None of the patients in either group experienced life-threatening or delayed complications during the follow-up period.
4. Discussion
The American Thyroid Association (ATA) encourages treatment de-escalation for low-risk PTC and supports AS for low-risk PTMC due to its indolent behavior and relatively favorable prognosis [Citation28]. However, the path toward implementing AS practices in China remains unclear. Major barriers to AS include negative emotions related to thyroid cancer, fear of disease progression without treatment, psychological struggles, and a lack of comprehensive understanding of AS [Citation29].
To date, no specific guidelines have been established for the treatment of low-risk isthmic PTC. The unique anatomic location of isthmic PTCs may limit the scope of AS for these tumors [Citation30]. In addition, the extent of thyroid resection and the role of prophylactic central neck dissection (PCND) for isthmic PTCs remain controversial. Many surgeons prefer total thyroidectomy and PCND for isthmic PTCs because of the high incidence of LNM, multifocality, and capsular invasion [Citation8–10]. However, those advocating isthmusectomy suggest that avoiding unnecessary extensive operations can reduce surgery-related complications and improve patients’ quality of life [Citation31,Citation32].
Minimally invasive thermal ablation has been used to treat patients with low-risk PTC and has yielded promising results [Citation12–16]. The latest clinical practice guidelines recommend thermal ablation for treating low-risk PTMC [Citation33]. However, the outcomes of thermal ablation for isthmic PTCs remain unclear. This study investigated the outcomes of RFA for low-risk isthmic PTC and compared them with those for lobe-originating PTC. Patients with isthmic and lobe-originating PTC treated with RFA showed similar LTP, LTPFS, volume change, VRR, and complication rates after PSM. To the best of our knowledge, this is the first study to compare the outcomes of RFA for isthmic- and lobe-originating PTC using PSM.
RFA is a local ablative therapy in which tumor tissues are destroyed in situ by coagulative necrosis and protein denaturation through frictional heating generated by tissue ionic agitation from high-frequency alternating current [Citation34]. After RFA, inflammatory cell infiltrates in the peripheral ablation zone and immune response is stimulated [Citation34]; subsequently, the coagulative necrosis was resorbed by the body, which demonstrated a gradual decrease in size over time on follow-up US (). The involution of the ablation zone varies depending on the RFA energy, tumor calcification, patients’ age and sex [Citation35]. Part of coagulative necrosis is replaced by fibrosis and scar tissue rather than disappearance over time, likely accounting for the presence of a persistent mass on follow-up US, which makes it difficult to differentiate from minor persistent lesions sometimes. Ma et al. [Citation36] retrospectively reported surgical confirmation of residual PTC in 12 patients after thermal ablation and suggested that thermal ablation may cause incomplete ablation. Therefore, confirming complete ablation is crucial in the RFA of low-risk PTC. The Chinese expert consensus recommended that the efficacy of thermal ablation should be evaluated by biopsy at an early stage after thermal ablation [Citation37]. Yan et al. [Citation38] confirmed that CNB could detect residual cancer cells early, and all positive CNB was found in the peripheral zone, which undergoes sublethal hyperthermia and may recover from reversible injury [Citation34]. To reduce tumor residue, the ablation zone extended at least 3 mm beyond the tumor margins [Citation23]. In this study, 80.8% of tumors in the isthmic group, as well as 76.9% in the lobar group, disappeared, while only 1.1% of persistent lesions were confirmed by biopsy. Therefore, a biopsy targeting the peripheral zone performed at an appropriate time after thermal ablation may bridge the gap between reducing unnecessary biopsies and missing persistent lesions.
In terms of LTP, only new tumors were observed in the isthmic group. This may be explained by the fact that isthmic PTC shows a higher incidence of multifocality than PTC confined to the thyroid lobes [Citation39]. The multiple microlesions that were not detected in the US during initial treatment could have developed into new tumors during the follow-up period. Lymph vessels from the isthmus typically drain into the pretracheal and prelaryngeal lymph nodes [Citation39]. However, the US demonstrates poor sensitivity in the diagnosis of central LNM [Citation40]. This may explain why isthmic PTC showed a lower incidence of LNM in our study. Lei et al. [Citation41] reported the findings for 103 patients who underwent total or less-than-total thyroidectomy, and five patients experienced recurrence after a median follow-up of 22 months (range, 2–54 months), which is comparable with our results. Other studies reported that the recurrence rate of isthmic PTC after surgery was 2.9–3.1% [Citation42,Citation43]; however, the follow-up period in those studies was longer than ours. Therefore, our results require further validation with long-term follow-up. As for LTPFS, no differences were observed in the Kaplan–Meier survival curves, but the LTPFS in the isthmic group tended to be lower than that in the lobar group, which also needs to be confirmed with a longer follow-up.
The most common major complication of RFA is RLN injury. Kim et al. reported that the incidence of RLN injury after RFA was 0.7% [Citation44], which was consistent with our results (1.0% after PSM). Because the thyroid lobes are closer to the RLN than to the isthmus, RLN injury is more likely to occur in lobe-originating PTC. While the hydrodissection technique can prevent heat injury, US guidance and physician experience can further reduce the occurrence of such injuries to some extent.
This study had some limitations. First, the number of patients included was small, and the mean follow-up period (28 months) was short, which may have been underpowered for such a slow-growing disease. Thus, additional large multicenter studies with long-term follow-up are required. Second, post-ablation histological examinations were not performed in all patients; therefore, the persistence of microresidual cancer cannot be ruled out. Third, comparison of patients treated with thyroid isthmusectomy and RFA may have been better. However, only a few patients with isthmic PTC underwent isthmusectomies at our institution.
In conclusion, the outcomes of RFA for low-risk isthmic PTC were similar to those observed for tumors located in the thyroid lobes. Therefore, RFA may be an option for select patients with low-risk isthmic PTC, particularly those who are ineligible for or refuse surgery. However, these findings should be confirmed over a long-term follow-up period. Pre- and post-ablation imaging studies are important for patients who undergo thermal ablation for low-risk isthmic PTC, because new tumors accounted for the majority of cases showing LTP in this study.
Supplemental Material
Download ()Acknowledgement
We are grateful to all the participants for their support in this study.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
Some or all datasets generated during and/or analyzed during the current study are not publicly available but are available from the corresponding author upon reasonable request.
Additional information
Funding
References
- Gandolfi G, Sancisi V, Piana S, et al. Time to re-consider the meaning of BRAF V600E mutation in papillary thyroid carcinoma. Int J Cancer. 2015;137(5):1001–1011. doi: 10.1002/ijc.28976.
- Megwalu UC, Moon PK. Thyroid cancer incidence and mortality trends in the United States: 2000-2018. Thyroid. 2022;32(5):560–570. doi: 10.1089/thy.2021.0662.
- Miranda-Filho A, Lortet-Tieulent J, Bray F, et al. Thyroid cancer incidence trends by histology in 25 countries: a population-based study. Lancet Diabetes Endocrinol. 2021;9(4):225–234. doi: 10.1016/S2213-8587(21)00027-9.
- Song Q, Gao H, Tian X, et al. Evaluation of ultrasound-guided radiofrequency ablation as a treatment option for papillary thyroid microcarcinoma in the isthmus: a retrospective study. Front Endocrinol. 2020;11:599471. doi: 10.3389/fendo.2020.599471.
- Goldfarb M, Rodgers SS, Lew JI. Appropriate surgical procedure for dominant thyroid nodules of the isthmus 1 cm or larger. Arch Surg. 2012;147(9):881–884. doi: 10.1001/archsurg.2012.728.
- Lee YS, Jeong JJ, Nam KH, et al. Papillary carcinoma located in the thyroid isthmus. World J Surg. 2010;34(1):36–39. doi: 10.1007/s00268-009-0298-6.
- Nixon IJ, Palmer FL, Whitcher MM, et al. Thyroid isthmusectomy for well-differentiated thyroid cancer. Ann Surg Oncol. 2011;18(3):767–770. doi: 10.1245/s10434-010-1358-8.
- Jasim S, Baranski TJ, Teefey SA, et al. Investigating the effect of thyroid nodule location on the risk of thyroid cancer. Thyroid. 2020;30(3):401–407. doi: 10.1089/thy.2019.0478.
- Vasileiadis I, Boutzios G, Karalaki M, et al. Papillary thyroid carcinoma of the isthmus: total thyroidectomy or isthmusectomy? Am J Surg. 2018;216(1):135–139. doi: 10.1016/j.amjsurg.2017.09.008.
- Ramundo V, Lamartina L, Falcone R, et al. Is thyroid nodule location associated with malignancy risk? Ultrasonography. 2019;38(3):231–235. doi: 10.14366/usg.18050.
- Wang TS, Sosa JA. Thyroid surgery for differentiated thyroid cancer - recent advances and future directions. Nat Rev Endocrinol. 2018;14(11):670–683. doi: 10.1038/s41574-018-0080-7.
- Zheng L, Dou JP, Liu FY, et al. Microwave ablation vs. surgery for papillary thyroid carcinoma with minimal sonographic extrathyroid extension: a multicentre prospective study. Eur Radiol. 2023;33(1):233–243. doi: 10.1007/s00330-022-08962-6.
- Yan L, Zhang M, Song Q, et al. Ultrasound-guided radiofrequency ablation versus thyroid lobectomy for low-risk papillary thyroid microcarcinoma: a propensity-matched cohort study of 884 patients. Thyroid. 2021;31(11):1662–1672. doi: 10.1089/thy.2021.0100.
- Kim HJ, Chung SM, Kim H, et al. Long-term efficacy of ultrasound-guided laser ablation for papillary thyroid microcarcinoma: results of a 10-year retrospective study. Thyroid. 2021;31(11):1723–1729. doi: 10.1089/thy.2021.0151.
- Cho SJ, Baek SM, Na DG, et al. Five-year follow-up results of thermal ablation for low-risk papillary thyroid microcarcinomas: systematic review and meta-analysis. Eur Radiol. 2021;31(9):6446–6456. doi: 10.1007/s00330-021-07808-x.
- Mauri G, Orsi F, Carriero S, et al. Image-guided thermal ablation as an alternative to surgery for papillary thyroid microcarcinoma: preliminary results of an Italian experience. Front Endocrinol (Lausanne). 2020;11:575152. doi: 10.3389/fendo.2020.575152.
- Cao XJ, Zhao ZL, Wei Y, et al. Microwave ablation for papillary thyroid cancer located in the thyroid isthmus: a preliminary study. Int J Hyperthermia. 2021;38(1):114–119. doi: 10.1080/02656736.2021.1880028.
- Zheng L, Liu FY, Yu J, et al. Thermal ablation for papillary thyroid microcarcinoma located in the isthmus: a study with 3 years of follow-up. Future Oncol. 2022;18(4):471–480. doi: 10.2217/fon-2021-0463.
- Mauri G, Pacella CM, Papini E, et al. Image-guided thyroid ablation: proposal for standardization of terminology and reporting criteria. Thyroid. 2019;29(5):611–618. doi: 10.1089/thy.2018.0604.
- Tessler FN, Middleton WD, Grant EG, et al. ACR thyroid imaging, reporting and data system (TI-RADS): white paper of the ACR TI-RADS committee. J Am Coll Radiol. 2017;14(5):587–595. doi: 10.1016/j.jacr.2017.01.046.
- Xiao J, Zhang Y, Yan L, et al. Ultrasonography-guided radiofrequency ablation for solitary T1aN0M0 and T1bN0M0 papillary thyroid carcinoma: a retrospective comparative study. Eur J Endocrinol. 2021;186(1):105–113. doi: 10.1530/EJE-21-0580.
- Kim JH, Baek JH, Lim HK, et al. 2017 Thyroid radiofrequency ablation guideline: Korean society of thyroid radiology. Korean J Radiol. 2018;19(4):632–655. doi: 10.3348/kjr.2018.19.4.632.
- Zhang M, Tufano RP, Russell JO, et al. Ultrasound-guided radiofrequency ablation versus surgery for low-risk papillary thyroid microcarcinoma: results of over 5 years’ follow-up. Thyroid. 2020;30(3):408–417. doi: 10.1089/thy.2019.0147.
- Cho SJ, Baek SM, Lim HK, et al. Long-term follow-up results of ultrasound-guided radiofrequency ablation for low-risk papillary thyroid microcarcinoma: more than 5-year follow-up for 84 tumors. Thyroid. 2020;30(12):1745–1751. doi: 10.1089/thy.2020.0106.
- Ahmed M, Solbiati L, Brace CL, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria–a 10-year update. Radiology. 2014;273(1):241–260. doi: 10.1148/radiol.14132958.
- Baek JH, Lee JH, Sung JY, et al. Complications encountered in the treatment of benign thyroid nodules with US-guided radiofrequency ablation: a multicenter study. Radiology. 2012;262(1):335–342. doi: 10.1148/radiol.11110416.
- Haukoos JS, Lewis RJ. The propensity score. JAMA. 2015;314(15):1637–1638. doi: 10.1001/jama.2015.13480.
- Haugen BR, Alexander EK, Bible KC, et al. 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association Guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid. 2016;26(1):1–133. doi: 10.1089/thy.2015.0020.
- Zhu P, Zhang Q, Wu Q, et al. Barriers and facilitators to the choice of active surveillance for low-risk papillary thyroid cancer in China: a qualitative study examining patient perspectives. Thyroid. 2023;33(7):826–834. doi: 10.1089/thy.2022.0347.
- Brito JP, Ito Y, Miyauchi A, et al. A clinical framework to facilitate risk stratification when considering an active surveillance alternative to immediate biopsy and surgery in papillary microcarcinoma. Thyroid. 2016;26(1):144–149. doi: 10.1089/thy.2015.0178.
- Kwon O, Lee S, Bae JS, et al. Thyroid isthmusectomy with prophylactic central compartment neck dissection is a feasible approach for papillary thyroid cancer on the isthmus. Ann Surg Oncol. 2021;28(11):6603–6612. doi: 10.1245/s10434-021-09833-y.
- Park H, Harries V, McGill MR, et al. Isthmusectomy in selected patients with well-differentiated thyroid carcinoma. Head Neck. 2020;42(1):43–49. doi: 10.1002/hed.25968.
- Mauri G, Hegedüs L, Bandula S, et al. European thyroid association and cardiovascular and interventional radiological society of Europe 2021 clinical practice guideline for the use of minimally invasive treatments in malignant thyroid lesions. Eur Thyroid J. 2021;10(3):185–197. doi: 10.1159/000516469.
- Chu KF, Dupuy DE. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer. 2014;14(3):199–208. doi: 10.1038/nrc3672.
- He H, Zhang Y, Song Q, et al. Nomogram prediction for the involution of the ablation zone after radiofrequency ablation treatment in patients with low-risk papillary thyroid carcinoma. Int J Hyperthermia. 2021;38(1):1133–1139. doi: 10.1080/02656736.2021.1960434.
- Ma B, Wei W, Xu W, et al. Surgical confirmation of incomplete treatment for primary papillary thyroid carcinoma by percutaneous thermal ablation: a retrospective case review and literature review. Thyroid. 2018;28(9):1134–1142. doi: 10.1089/thy.2017.0558.
- Ge M, Xu D, Yang A, et al. Expert consensus on thermal ablation for thyroid benign nodes, microcarcinoma and metastatic cervical lymph nodes (2018 edition). China Cancer. 2018;27:768–773.
- Yan L, Luo Y, Zhang Y, et al. The clinical application of core-needle biopsy after radiofrequency ablation for low-risk papillary thyroid microcarcinoma: a large cohort of 202 patients study. J Cancer. 2020;11(18):5257–5263. doi: 10.7150/jca.42673.
- Karatzas T, Charitoudis G, Vasileiadis D, et al. Surgical treatment for dominant malignant nodules of the isthmus of the thyroid gland: a case control study. Int J Surg. 2015;18:64–68. doi: 10.1016/j.ijsu.2015.04.039.
- Zhao H, Li H. Meta-analysis of ultrasound for cervical lymph nodes in papillary thyroid cancer: diagnosis of central and lateral compartment nodal metastases. Eur J Radiol. 2019;112:14–21. doi: 10.1016/j.ejrad.2019.01.006.
- Lei J, Zhu J, Li Z, et al. Surgical procedures for papillary thyroid carcinoma located in the thyroid isthmus: an intention-to-treat analysis. Onco Targets Ther. 2016;9:5209–5216. doi: 10.2147/OTT.S106837.
- Gui Z, Wang Z, Xiang J, et al. Comparison of outcomes following thyroid isthmusectomy, unilateral thyroid lobectomy, and total thyroidectomy in patients with papillary thyroid microcarcinoma of the thyroid isthmus: a retrospective study at a single center. Med Sci Monit. 2020;26:e927407. doi: 10.12659/MSM.927407.
- Huang H, Yan D, Liu W, et al. Isthmectomy is effective and sufficient for selected patients with the isthmus-confined solitary papillary thyroid carcinoma. Asian J Surg. 2022;45(9):1678–1681. doi: 10.1016/j.asjsur.2021.08.074.
- Kim C, Lee JH, Choi YJ, et al. Complications encountered in ultrasonography-guided radiofrequency ablation of benign thyroid nodules and recurrent thyroid cancers. Eur Radiol. 2017;27(8):3128–3137. doi: 10.1007/s00330-016-4690-y.