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Changing Trends of Thyroid Cancer Clinical Characteristics and Treatment Pattern in South Korea: Insights from an Institutional Database and the Korean Cancer Center Registry Database
Int J Thyroidol 2024;17(2):277-285
Published online November 30, 2024;  https://doi.org/10.11106/ijt.2024.17.2.277
© 2024 Korean Thyroid Association.

Yung Jee Kang1,2*, Nayeon Choi1*, Jungirl Seok2,3, Sun Wook Kim4, Tae-Hyuk Kim4, Jae Hoon Chung4, Young-Ik Son1 and Man Ki Chung1

Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine1, Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul National University College of Medicine2, Seoul, Department of Otorhinolaryngology-Head and Neck Surgery, National Cancer Center3, Goyang, Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine4, Seoul, Korea
Correspondence to: Man Ki Chung, MD, PhD, Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea
Tel: 82-2-3410-1845, Fax: 82-2-3410-6789, E-mail: chungmk@skku.edu

Young-Ik Son, MD, PhD, Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea
Tel: 82-2-3410-3579, Fax: 82-2-3410-3879, E-mail: yison@skku.edu

*These authors contributed equally to this work.
Received February 8, 2024; Accepted July 12, 2024.
This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background and Objectives: To analyze the clinical trends and treatment patterns of thyroid cancer in the recent decade in South Korea. Materials and Methods: Two distinctive datasets, a single institutional database from 2009 to 2021 of differentiated thyroid cancer (DTC) patients (n=3145) and a nationwide database of the Korean Cancer Center Registry (KCCR) from 2005 to 2019 for patients (n=414,828) with all types of thyroid cancer, were analyzed. Annual incidence, the extent of thyroidectomy and neck dissection, T and N stages, and postoperative radioactive iodine (RAI) were investigated and descriptively presented. Results: The institutional database demonstrated that the annual cases of DTC surgeries suddenly dropped in 2014, coinciding with a social debate on overdiagnosis in South Korea. Due to changes in the staging manual and management guidelines during the study period, lobectomy has been preferred more than total thyroidectomy and the number of anterior compartment neck dissections has decreased. However, cases with lateral neck dissection and T4 stage gradually increased, suggesting that social issue did not influence the incidence of advanced thyroid diseases. The KCCR database also supported a similar phenomenon that showed a recent increase in localized and regional disease after a shock from social controversy. Conclusion: Our institutional and KCCR data findings collectively indicate a steady incidence in localized and regional thyroid cancer after the initial drop triggered by the 2014 controversy in South Korea.
Keywords : Thyroid neoplasms, Incidence, Surgery, Treatment, Database
Introduction

The global incidence of thyroid cancer has notably risen in recent decades. This is primarily attributed to enhanced diagnostic capabilities such as ultrasonography (US) and active screening programs.1-5) The increased incidence of thyroid cancer predominantly reflects the detection of subclinical thyroid disease rather than a genuine surge in thyroid cancer cases.4,6,7) This trend has raised concerns about the overdiagnosis and overtreatment of thyroid cancer, a phenomenon observed in several countries, including the United States, Italy, France, Australia, and South Korea.3,8,9) In South Korea, the national incidence of thyroid cancer has steadily increased, reaching its peak in 2012. However, it subsequently declined following a social debate regarding the overdiagnosis issue in 2014. This debate stemmed from the heightened awareness of detecting indolent thyroid cancers that might not require aggressive treatment.10-12)

In a recent decade, significant shifts have occurred in thyroid cancer treatment strategies due to updates of cancer staging systems and management guidelines.13,14) The revised cancer staging manual emphasizes appropriate risk stratification, categorizing most differentiated thyroid cancer (DTC) patients as low risk for mortality. Consequently, management guidelines recommend less extensive surgeries such as lobectomy for low-risk patients. Therefore, it would be critical to review impacts of the above-mentioned factors on thyroid cancer trends to assess the current situation and predict the future trends. However, there is little report on this issue from South Korea.

The present study aims to provide updated insights into the incidence and patterns of thyroid cancer surgery over the past decade, assess whether surgical trends correlate with changes in staging manuals and management guidelines, and evaluate trend changes after the social debate on overdiagnosis of thyroid cancer in South Korea.

Materials and Methods

Data Sources

Data for thyroid cancer surgery incidence were collected from two different sources: our institutional cancer registry (SMC) and the Korean Central Cancer Registry (KCCR). The institutional registry allowed for an in-depth analysis of thyroid cancer surgery changes, while the KCCR database corroborated nationwide trends. Ethical approval was obtained from the Institutional Review Board (IRB) of Samsung Medical Center (SMC) (SMC-IRB No. 2022-07-010).

For the institutional dataset, we identified and reviewed all patients consecutively treated for DTC between January 2009 and December 2021. After excluding cases with incomplete records or loss to follow-up, 3145 patients remained for analysis. Demographic and clinicopathological data including age, gender, TNM classification, surgical extent, invasion of adjacent structures, and oncological outcomes were assessed.

The KCCR database aggregates data from hospital-based regional cancer registries and provides annual nationwide cancer incidence, survival, and prevalence statistics.15) A total of 414,828 patients diagnosed with thyroid cancer cases between 2005 and 2018 were identified using the International Classification of Diseases for Oncology (ICD-O) topography code C73.16) Histological subtypes were classified as papillary thyroid carcinoma (morphology codes: 8050, 8260, 8340-8344, 8350, 8450-8460), follicular thyroid carcinoma (morphology codes: 8290, 8330-8335), medullary thyroid carcinoma (morphology codes: 8345, 8510-8513), anaplastic thyroid carcinoma (morphology codes: 8020-8035), and others according to the ICD-O. The stage was assessed by the Surveillance, Epidemiology, and End Results (SEER) summary stage, which was classified into localized (cancer located within the original organ and not found elsewhere), regional (cancer invading the regional lymph node or organ located around the origin, without remote metastasis), distant (cancer fallen away from the primary organ and spread to other tissues far away), and unknown stages.

Treatment and Follow-Up

Surgical treatment protocol of DTC in our institution was as follows. Preoperative evaluations included physical examination, laryngoscopy and US to assess characteristics of the primary tumor as well as lymph node status in the central compartment and lateral neck (which was accompanied by fine needle aspiration biopsies on the clinician and radiologist’s decision), and contrast-enhanced computed tomography (CECT) or magnetic resonance imaging in patients with suspicious tumor invasion into adjacent structures.

The appropriate surgical extent was determined based on management guidelines.13,17) Anterior compartment neck dissection (ACND) comprised of level VI and lateral neck dissection (LND) encompassed the anterior compartment and neck level II-V. Using a multidisciplinary team approach, the necessity for and intensity of postoperative adjuvant therapy was determined by stratifying individual risk based on patient demographics, surgical findings, and pathologic reports.

Postoperative follow-up periods were equalized to 2 years. Recurrence patterns and the period to recurrence were investigated. Recurrence was determined when clinically suspected or pathologically proven tumors were found in the thyroidectomy bed (local), lateral neck (regional), or distant sites (distant metastasis).

Statistical Analysis

The primary analysis of the present study was to evaluate changing trends in overall annual cases and the extent of surgery for thyroid cancer over nearly a decade. Second, we assess whether surgical trends correlated with changes in staging manuals and management guidelines and to evaluate trends after social debate on overdiagnosis of thyroid cancer.

Trends in T and N classification, surgical treatment, and postoperative radioactive iodine (RAI) for DTC over the past 10 years were graphically depicted, focusing on descriptive statistical analysis rather than statistical significance. AJCC 7th edition TNM classification was used until 2016, transitioning to the 8th edition from 2017 onwards.

Results

Table 1 presents patients’ clinical and surgical characteristics with DTC in the institutional database. The average age of patients was 48.1 years, with a majority (71.3%) being females (2241 out of 3145 patients). Regarding tumor staging, 52.9% had T1-2 tumors and 47.1% had T3-4 tumors. Lymph node involvement was observed in 40.2% (N1) but absent in 59.8% (N0). Surgical procedures included hemithyroidectomy in 39.8% and total thyroidectomy in 60.2% of cases. ACND was performed in 45.3%, while LND was done in 18.6% of cases. Postoperative RAI was administered to 52.2% of patients, while 47.8% did not receive RAI. As of the last follow-up, 66 cases had local recurrence, 104 had regional recurrence, and 12 had distant metastasis, with a mean time to recurrence of 21.9±4.7 months.

Study patients of the institutional database (n=3145)

Variable
Age, year, mean±Std 48.1±12.1
Sex, male/female (%) 904 (28.7)/2241 (71.3)
TNM staging (%)*
T1-2/T3-4 1664 (52.9)/1421 (47.1)
N0/N1 1881 (59.8)/1264 (40.2)
Thyroidectomy extent (%)
Hemithyroidectomy 1254 (39.8)
Total thyroidectomy 1909 (60.2)
Neck dissection extent (%)
No 1137 (36.1)
ACND 1425 (45.3)
LND 601 (18.6)
Postoperative RAI (%)
No 1504 (47.8)
Yes 1659 (52.2)
Failure pattern
Local recurrence 66
Regional recurrence 104
Distant metastasis 12
Time to recurrence, month,
mean±Std		 21.9±4.7

ACND: anterior compartment neck dissection, LND: lateral neck dissection, RAI: radioactive iodine, Std: standard deviation

*AJCC 7th edition until 2016, 8th edition after 2017.

Fig. 1 presents annual cases of DTC surgeries from 2009 to 2021, demonstrating a sudden drop in 2014 to be below 200 cases per year. This coincided with a social debate on overdiagnosis and overtreatment of thyroid cancer in South Korea. Since then, the number has hovered around 100 cases yearly, with a gradual increase recently.

Fig. 1. Annual cases of DTC surgery based on the database of a single institution from 2009 to 2021. The number of DTC surgeries showed a sudden dropped in 2014 with a gradual recent increase.

Fig. 2A illustrates changes in thyroidectomy extent, showing a gradual decrease in total thyroidectomy and an increase in lobectomy. This shift was influenced by revised thyroid nodule management guidelines in the United States and South Korea in 2016 and 2017, respectively, expanding lobectomy indications. Significant changes in T stage and surgical extent were observed during the study period as depicted in Fig. 2B. T1 and T3 stages predominated between 2009 and 2017. However, a notable decrease in T3 stage occurred in 2018, coinciding with revision of the AJCC staging manual, as a microscopic extra-thyroid extension of the tumor was excluded from the T3 category in the 8th edition. On the contrary, T4 stage incidence increased, with a sudden spike in 2021. Although overall surgery cases decreased, the proportion of T4 stage cases gradually increased, accounting for nearly 10% of total cases last year. Detailed surgical information of T4 stage disease is summarized in Table 2, including invasion into adjacent structures: the larynx/trachea, the recurrent laryngeal nerve (RLN), soft tissue, and combined cases. It is noteworthy that the types and numbers of invaded structures by T4 tumors did not change throughout the study period.

Annual cases of adjacent structure invasion in T4 stage differentiated thyroid cancer

2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020 2021
Larynx/trachea 2 1 0 3 6 1 2 3 2 1 0 1 10
RLN 0 1 6 5 6 5 1 1 1 1 3 2 1
Soft tissue 0 0 3 0 0 0 1 0 0 1 0 2 1
Combined 0 1 2 2 0 0 1 0 0 1 2 0 0
Total 2 3 11 10 12 6 5 4 3 4 5 5 12

RLN: recurrent laryngeal nerve

*AJCC 7th edition until 2016, 8th edition after 2017.

Fig. 2. Annual changes of surgical extent and T classification from 2009 to 2021 in DTC. (A) Annual changes of the extent of thyroidectomy, showing a gradual decrease in total thyroidectomy and an increase in lobectomy. (B) Annual changes in proportion of T classification. While T3 stage was notably decreased in 2018, incidence of T4 stage was suddenly increased in 2021.

Regarding the N stage, Fig. 3A indicates no significant difference in N0 or N1 frequency throughout the study period. However, Fig. 3B demonstrates a substantial change in neck management type, with a decrease in ACND frequency since 2015 and a sharp increase in LND, which was performed mostly for therapeutic purposes, in the last year. Fig. 4 shows a steady decrease in postoperative RAI incidence due to these surgical strategy changes.

Fig. 3. Annual changes of N classification and surgical extent from 2009 to 2021 in DTC. (A) Annual changes in proportion of N classification. There was no definite difference in N0 or N1 frequency. (B) Annual changes in the extent of neck management. Frequency of ACND decreased since 2015, while frequency of LND sharply increased.

Fig. 4. Annual number of postoperative RAI from 2009 to 2021. Postoperative RAI incidence steadily decreased over that period.

In a brief summary, our analysis of 3145 DTC patients from the institutional database between 2009 and 2021 highlights a surgical trend towards less extensive surgery such as lobectomy over total thyroidectomy and no ACND over prophylactic ACND. This shift was influenced by the revision of the cancer staging manual and management guidelines, alongside a sudden drop in overall DTC incidence after the controversy surrounding DTC overdiagnosis in South Korea. However, it was also noticeable that the number of therapeutic LND and the proportion of advanced T stage tumors had steadily increased throughout the study period. This finding suggests that the number of advanced thyroid disease has not been affected by the shock from the social debate in South Korea, emphasizing the importance of precise preoperative evaluation and careful patient counseling.

From the analysis of the KCCR database with 414,828 patient records from 2005 to 2018 (Fig. 5A), it showed a continuous increase in thyroid cancer incidence nationwide until 2012, followed by a sudden decrease in 2014 and 2015 due to social controversy. Subsequently, the decreased incidence remained stable until 2018. Fig. 5B reveals a decrease in localized and regional disease after 2012 with a recent increase in the later study period.

Fig. 5. Thyroid cancer registration data from the Korea National Cancer Center. (A) Changes of total number in both differentiated and undifferentiated thyroid cancer surgery from 2005 to 2018. Thyroid cancer incidence continuously increased until 2012, with a sudden decrease in 2014 and 2015. Its incidence remained stable until 2018. (B) Incidence of thyroid cancer according to localized, regional, distant metastasis and is unknown. Localized and regional disease decreased after 2012 with a recent increase until 2018.

Taken together, our institutional database and the KCCR cancer registry collectively indicated a steady increase in localized and regional thyroid cancer incidence after the initial drop triggered by the 2014 controversy in South Korea. Despite an increased application of lobectomy, T4 stage tumors and lateral neck metastatic disease have increased, warranting careful evaluation and counseling in treatment planning.

Discussion

In the present study, a trend analysis was performed using institutional and KCCR nationwide databases to investigate clinical characteristics of thyroid cancer and treatment pattern changes in the recent decade in South Korea. Our analysis highlighted a trend towards less extensive surgery (lobectomy and no ACND), alongside a sudden drop in overall thyroid cancer cases after the social debate over the overdiagnosis in South Korea. Interestingly, there was a gradual increase in the proportion of LND and T4 stage tumors in the institutional database and the proportion of localized and regional disease in the KCCR database. These findings indicated that the shock from the social debate did not affect the number of advanced thyroid disease in South Korea, despite trend changes to more conservatory surgeries.

Previous studies from other countries have dealt with the relationship between overdiagnosis issue and thyroid cancer incidence. In Russia, not only an exposure to iodine 131, which is a significant factor affecting the increase of thyroid cancer incidence, but also overdiagnosis using US screening could increase thyroid cancer prevalence.18) Other countries including India, Italy, and the United States have reported an increase in thyroid cancer possibly from active screening of small, indolent tumors by US.3,8,9,18,19) South Korea is one of the several countries where a social controversy over the overdiagnosis and overtreatment of DTC has strongly affected overall cancer trends.12) Interestingly, it has been reported that the incidence of thyroid cancer in South Korea has begun to decline from 2012, before the social debate in 2014.20) Authors attributed this phenomenon to changes in management guidelines for thyroid nodule examinations accelerated by debates. However, it is obvious that the incidence is bouncing back and increasing after a short period of drop. It is assumed that an increase of surgical cases for small, low-risk thyroid cancer is the main reason of the re-increasing trend of thyroid cancer in South Korea.21) These findings support outcomes of the present study, showing that the recent increase of localized and regional disease is distinctive after a shock from the social debate. Future studies are necessary to assess other reasons for the re-increase of the incidence, such as cancer screening with US.

A few studies have covered changes in trends and treatment patterns after the social controversy about the overdiagnosis issue. In the United States, the SEER registry showed that thyroid cancer incidence decreased after overdiagnosis issue during 2014 to 2018, similar to South Korea.22) It was noteworthy that the incidence of tumors of less than 1.0 cm was declined, but not for tumors larger than 2.0 cm during 2015-2018. In addition, mortality due to thyroid cancer was found to continue to increase, particularly for papillary thyroid cancer larger than 2 cm and for distant diseases, suggesting that changes in practice patterns did not affected the incidence of more advanced tumors. This finding was similar to the present study, as the number of LND and T4 stage tumor remained stable or slightly increased after the incidence drop in South Korea. Consistent incidence of advanced thyroid cancer cases despite changes in guidelines and overall incidence suggests that careful evaluation of disease extent at initial work-up must not be mitigated by more conservatively changed guidelines.

Management guidelines have evolved, reflecting social issues of overdiagnosis and overtreatment in DTC.13,23-25) In consequence, increasing proportion of thyroid lobectomy from 17% to 24% during the period of 2015 to 2018 was observed from a study in the United States.26) Declining RAI management of low-risk adult PTC corresponded with the recent ATA practice guidelines.26,27) These findings are consistent with the present study. Debates about prophylactic central neck dissection in cN0 patients and the extent of therapeutic LND are continued.28) Trends in the incidence of therapeutic LND in DTC is not well reported. Therefore, our study has an advantage in that it reports the trend in the incidence of neck dissection.

Our study has several limitations that warrant consideration. Firstly, this was a retrospective analysis of two different database sets, with several mismatches between the two data sets because data retrieval was performed differently. For example, study periods did not align precisely between the two databases (a period gap in data from 2019 to 2021). Also, the KCCR encompasses all types of thyroid cancers, while the institutional database included the DTC only. The KCCR did not provide detailed information on disease extent or surgery type as the institutional database. Therefore, further investigations are imperative to draw broader conclusions applicable worldwide, encompassing diverse geographical regions and healthcare settings. Secondly, our study primarily employed descriptive statistics rather than delving into statistical significance. This approach provides a broad overview of trends and patterns. However, it does not indicate statistical precisions. Thirdly, our analysis predominantly focused on DTC’s incidence and surgical trends over the recent decade. However, we did not investigate oncological outcomes or survival rates concerning shifts in treatment paradigms and incidence rates. Future studies should aim to comprehensively analyze both the incidence and oncological outcomes associated with DTC.

Nonetheless, our findings highlight a persistent incidence of locally advanced and regionally metastatic thyroid cancer in South Korea. This trend remains despite a sudden drop in the incidence after the social debate surrounding overdiagnosis and changes of staging manual and guidelines on thyroid cancer. Physicians must carefully evaluate disease extent and counsel patients about proper treatment options and the follow-up scheme. Results of the present study carry significance as they suggest a potential shift in the future paradigm of thyroid cancer management. Further research is essential to elucidate and contextualize these evolving trends.

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

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