Endocrinology and Metabolism

Special Article

Miscellaneous
Immune Checkpoint Inhibitors and Endocrine Disorders: A Position Statement from the Korean Endocrine Society: Hyemi Kwon, Eun Roh, Chang Ho Ahn, Hee Kyung Kim, Cheol Ryong Ku, Kyong Yeun Jung, Ju Hee Lee, Eun Heui Kim, Sunghwan Suh, Sangmo Hong, Jeonghoon Ha, Jun Sung Moon, Jin Hwa Kim, Mi-kyung Kim, The Committee of Clinical Practice Guideline of the Korean Endocrine Society; Endocrinol Metab. 2022;37(6):839-850. Published online December 26, 2022; DOI: https://doi.org/10.3803/EnM.2022.1627

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Immune checkpoint inhibitors (ICIs) including an anti-cytotoxic T-lymphocyte-associated antigen 4 inhibitor, anti-programmed cell death protein 1 (PD-1) inhibitors, and anti-PD-ligand 1 inhibitors are representative therapeutics for various malignancies. In oncology, the application of ICIs is currently expanding to a wider range of malignancies due to their remarkable clinical outcomes. ICIs target immune checkpoints which suppress the activity of T-cells that are specific for tumor antigens, thereby allowing tumor cells to escape the immune response. However, immune checkpoints also play a crucial role in preventing autoimmune reactions. Therefore, ICIs targeting immune checkpoints can trigger various immune-related adverse events (irAEs), especially in endocrine organs. Considering the endocrine organs that are frequently involved, irAEs associated endocrinopathies are frequently life-threatening and have unfavorable clinical implications for patients. However, there are very limited data from large clinical trials that would inform the development of clinical guidelines for patients with irAEs associated endocrinopathies. Considering the current clinical situation, in which the scope and scale of the application of ICIs are increasing, position statements from clinical specialists play an essential role in providing the appropriate recommendations based on both medical evidence and clinical experience. As endocrinologists, we would like to present precautions and recommendations for the management of immune-related endocrine disorders, especially those involving the adrenal, thyroid, and pituitary glands caused by ICIs.

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Pembrolizumab plus lenvatinib for radically unresectable or metastatic renal cell carcinoma in the Japanese population
Ryo Fujiwara, Takeshi yuasa, kenichi kobayashi, tetsuya yoshida, susumu kageyama
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Incidence of Endocrine-Related Dysfunction in Patients Treated with New Immune Checkpoint Inhibitors: A Meta-Analysis and Comprehensive Review
Won Sang Yoo, Eu Jeong Ku, Eun Kyung Lee, Hwa Young Ahn
Endocrinology and Metabolism.2023; 38(6): 750. CrossRef

Original Article

Thyroid
Whole-Exome Sequencing in Papillary Microcarcinoma: Potential Early Biomarkers of Lateral Lymph Node Metastasis: Mijin Kim, Chae Hwa Kwon, Min Hee Jang, Jeong Mi Kim, Eun Heui Kim, Yun Kyung Jeon, Sang Soo Kim, Kyung-Un Choi, In Joo Kim, Meeyoung Park, Bo Hyun Kim; Endocrinol Metab. 2021;36(5):1086-1094. Published online October 28, 2021; DOI: https://doi.org/10.3803/EnM.2021.1132

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Background
Early identification of patients with high-risk papillary thyroid microcarcinoma (PTMC) that is likely to progress has become a critical challenge. We aimed to identify somatic mutations associated with lateral neck lymph node (LN) metastasis (N1b) in patients with PTMC.
Methods
Whole-exome sequencing (WES) of 14 PTMCs with no LN metastasis (N0) and 13 N1b PTMCs was performed using primary tumors and matched normal thyroid tissues.
Results
The mutational burden was comparable in N0 and N1b tumors, as the median number of mutations was 23 (range, 12 to 46) in N0 and 24 (range, 12 to 50) in N1b PTMC (P=0.918). The most frequent mutations were detected in PGS1, SLC4A8, DAAM2, and HELZ in N1b PTMCs alone, and the K158Q mutation in PGS1 (four patients, Fisher’s exact test P=0.041) was significantly enriched in N1b PTMCs. Based on pathway analysis, somatic mutations belonging to the receptor tyrosine kinase-RAS and NOTCH pathways were most frequently affected in N1b PTMCs. We identified four mutations that are predicted to be pathogenic in four genes based on Clinvar and Combined Annotation-Dependent Depletion score: BRAF, USH2A, CFTR, and PHIP. A missense mutation in CFTR and a nonsense mutation in PHIP were detected in N1b PTMCs only, although in one case each. BRAF mutation was detected in both N0 and N1b PTMCs.
Conclusion
This first comprehensive WES analysis of the mutational landscape of N0 and N1b PTMCs identified pathogenic genes that affect biological functions associated with the aggressive phenotype of PTMC.

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Special Article

Miscellaneous
COVID-19 Vaccination for Endocrine Patients: A Position Statement from the Korean Endocrine Society: Cheol Ryong Ku, Kyong Yeun Jung, Chang Ho Ahn, Jun Sung Moon, Ju Hee Lee, Eun Heui Kim, Hyemi Kwon, Hee Kyung Kim, Sunghwan Suh, Sangmo Hong, Jeonghoon Ha, Eun Roh, Jin Hwa Kim, Mi-kyung Kim, the Committee of Clinical Practice Guideline of the Korean Endocrine Society; Endocrinol Metab. 2021;36(4):757-765. Published online August 17, 2021; DOI: https://doi.org/10.3803/EnM.2021.404

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Since the first outbreak of coronavirus disease 2019 (COVID-19), ongoing efforts have been made to discover an efficacious vaccine against COVID-19 to combat the pandemic. In most countries, both mRNA and DNA vaccines have been administered, and their side effects have also been reported. The clinical course of COVID-19 and the effects of vaccination against COVID-19 are both influenced by patients’ health status and involve a systemic physiological response. In view of the systemic function of endocrine hormones, endocrine disorders themselves and the therapeutics used to treat them can influence the outcomes of vaccination for COVID-19. However, there are very limited data to support the development of clinical guidelines for patients with specific medical backgrounds based on large clinical trials. In the current severe circumstances of the COVID-19 pandemic, position statements made by clinical specialists are essential to provide appropriate recommendations based on both medical evidence and clinical experiences. As endocrinologists, we would like to present the medical background of COVID-19 vaccination, as well as precautions to prevent the side effects of COVID-19 vaccination in patients with specific endocrine disorders, including adrenal insufficiency, diabetes mellitus, osteoporosis, autoimmune thyroid disease, hypogonadism, and pituitary disorders.

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Shichen Xu, Huixin Yu, Xian Cheng, Jing Wu, Jiandong Bao, Li Zhang
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Yukako Kurematsu, Takako Mohri, Sadanori Okada, Yutaka Takahashi
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Original Articles

Clinical Study
Association between Serum Free Thyroxine and Anemia in Euthyroid Adults: A Nationwide Study: Mijin Kim, Bo Hyun Kim, Hyungi Lee, Min Hee Jang, Jeong Mi Kim, Eun Heui Kim, Yun Kyung Jeon, Sang Soo Kim, In Joo Kim; Endocrinol Metab. 2020;35(1):106-114. Published online March 19, 2020; DOI: https://doi.org/10.3803/EnM.2020.35.1.106

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Background

Studies on the relationship between thyroid function and anemia in the euthyroid range are scarce. We aimed to evaluate the association between anemia and serum free thyroxine (fT4) and thyrotropin (TSH) in euthyroid adults.

Methods

Data on 5,352 participants aged ≥19 years were obtained from the Korea National Health and Nutrition Examination Survey VI (2013 to 2015). Anemia was defined as hemoglobin (Hb) <13 and <12 g/dL for men and women, respectively.

Results

Overall, 6.1% of participants had anemia, and more women (9.9%) had anemia than men (2.8%, P<0.001). In multivariate analysis, serum fT4 levels, but not TSH, were positively associated with serum Hb levels in both sexes (P<0.001, each). Serum Hb levels linearly reduced across decreasing serum fT4 quartile groups in both sexes (P<0.001, each). After adjusting for potential confounding factors, participants with low-normal fT4 had 4.4 (P=0.003) and 2.8 times (P<0.001) higher risk for anemia than those with high-normal fT4 among men and women, respectively. When participants were divided into two groups at 50 years of age, in younger participants, men and women with the first quartile were at higher risk of anemia than men with the second quartile (odds ratio [OR], 3.3; P=0.029) and women with the forth quartile (OR, 3.2; P<0.001), respectively. This association was not observed in older participants.

Conclusion

These results suggest that a low-normal level of serum fT4 was associated with a lower serum Hb level and a higher risk of anemia in euthyroid adults, especially in younger participants.

Citations

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Thyroid Function and Risk of Anemia: A Multivariable-Adjusted and Mendelian Randomization Analysis in the UK Biobank
Nicolien A van Vliet, Annelies E P Kamphuis, Wendy P J den Elzen, Gerard J Blauw, Jacobijn Gussekloo, Raymond Noordam, Diana van Heemst
The Journal of Clinical Endocrinology & Metabolism.2022; 107(2): e643. CrossRef
Thyroid function, pernicious anemia and erythropoiesis: a two-sample Mendelian randomization study
Alisa D Kjaergaard, Alexander Teumer, Eirini Marouli, Panos Deloukas, Aleksander Kuś, Rosalie Sterenborg, Bjørn O Åsvold, Marco Medici, Christina Ellervik
Human Molecular Genetics.2022; 31(15): 2548. CrossRef
Changes of hematological indices in patients with diffuse toxic goiter
F. H. Saidova, L. M. Ahmedova, Zh. B. Aslanova, N. A. Najafov
Klinicheskaia khirurgiia.2021; 88(3-4): 76. CrossRef
Association between Serum Free Thyroxine and Anemia in Euthyroid Adults: A Nationwide Study (Endocrinol Metab 2020;35:106-14, Mijin Kim et al.)
Zheng Feei Ma
Endocrinology and Metabolism.2020; 35(2): 484. CrossRef
Association between Serum Free Thyroxine and Anemia in Euthyroid Adults: A Nationwide Study (Endocrinol Metab 2020;35:106-14, Mijin Kim et al.)
Mijin Kim, Bo Hyun Kim
Endocrinology and Metabolism.2020; 35(3): 669. CrossRef

Clinical Study
Disease-Specific Mortality of Differentiated Thyroid Cancer Patients in Korea: A Multicenter Cohort Study: Min Ji Jeon, Won Gu Kim, Tae Hyuk Kim, Hee Kyung Kim, Bo Hyun Kim, Hyon-Seung Yi, Eun Sook Kim, Hosu Kim, Young Nam Kim, Eun Heui Kim, Tae Yong Kim, Sun Wook Kim, Ho-Cheol Kang, Jae Hoon Chung, Young Kee Shong, Won Bae Kim; Endocrinol Metab. 2017;32(4):434-441. Published online November 22, 2017; DOI: https://doi.org/10.3803/EnM.2017.32.4.434

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Background

Little is known regarding disease-specific mortality of differentiated thyroid cancer (DTC) patients and its risk factors in Korea.

Methods

We retrospectively reviewed a large multi-center cohort of thyroid cancer from six Korean hospitals and included 8,058 DTC patients who underwent initial surgery between 1996 and 2005.

Results

Mean age of patients at diagnosis was 46.2±12.3 years; 87% were females. Most patients had papillary thyroid cancer (PTC; 97%) and underwent total thyroidectomy (85%). Mean size of the primary tumor was 1.6±1.0 cm. Approximately 40% of patients had cervical lymph node (LN) metastases and 1.3% had synchronous distant metastases. During 11.3 years of follow-up, 150 disease-specific mortalities (1.9%) occurred; the 10-year disease-specific survival (DSS) rate was 98%. According to the year of diagnosis, the number of disease-specific mortality was not different. However, the rate of disease-specific mortality decreased during the study period (from 7.7% to 0.7%). Older age (≥45 years) at diagnosis, male, follicular thyroid cancer (FTC) versus PTC, larger tumor size (>2 cm), presence of extrathyroidal extension (ETE), lateral cervical LN metastasis, distant metastasis and tumor node metastasis (TNM) stage were independent risk factors of disease-specific mortality of DTC patients.

Conclusion

The rate of disease-specific mortality of Korean DTC patients was 1.9%; the 10-year DSS rate was 98% during 1996 to 2005. Older age at diagnosis, male, FTC, larger tumor size, presence of ETE, lateral cervical LN metastasis, distant metastasis, and TNM stages were significant risk factors of disease-specific mortality of Korean DTC patients.

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Log odds of negative lymph nodes/T stage ratio (LONT): A new prognostic tool for differentiated thyroid cancer without metastases in patients aged 55 and older
Xuezhen Wang, Yufan Wu, Xiaoxia Li, Jinsheng Hong, Mingwei Zhang
Frontiers in Endocrinology.2023;[Epub] CrossRef
The association between vitamin D supplementation and the long-term prognosis of differentiated thyroid cancer patients: a retrospective observational cohort study with propensity score matching
Jong-hyuk Ahn, Hoonsung Choi, Su-jin Kim, Sun Wook Cho, Kyu Eun Lee, Do Joon Park, Young Joo Park
Frontiers in Endocrinology.2023;[Epub] CrossRef
Linear association between radioactive iodine dose and second primary malignancy risk in thyroid cancer
Kyeong Jin Kim, Kyoung Jin Kim, Jimi Choi, Nam Hoon Kim, Sin Gon Kim
JNCI: Journal of the National Cancer Institute.2023; 115(6): 695. CrossRef
Outcomes of Advanced Medullary Thyroid Carcinoma in the Era of Targeted Therapy
Nicholas L. Kesby, Alexander J. Papachristos, Matti Gild, Ahmad Aniss, Mark S. Sywak, Roderick Clifton-Bligh, Stan B. Sidhu, Anthony R. Glover
Annals of Surgical Oncology.2022; 29(1): 64. CrossRef
Clinical Implication of Mutifocality for Risk of Recurrence in Patients With Papillary Thyroid Carcinoma
Kwangsoon Kim, Ja Seong Bae, Jeong Soo Kim
Journal of Endocrine Surgery.2022; 22(1): 10. CrossRef
Clinical Factors Predictive of Lymph Node Metastasis in Thyroid Cancer Patients: A Multivariate Analysis
Hui Zheng, Victoria Lai, Jana Lu, Jin K Kang, Jiling Chou, Kenneth D Burman, Leonard Wartofsky, Jennifer E Rosen
Journal of the American College of Surgeons.2022; 234(4): 691. CrossRef
Minimal extrathyroidal extension is associated with lymph node metastasis in single papillary thyroid microcarcinoma: a retrospective analysis of 814 patients
Ra-Yeong Song, Hee Sung Kim, Kyung Ho Kang
World Journal of Surgical Oncology.2022;[Epub] CrossRef
Central Lymph Node Ratio Predicts Recurrence in Patients with N1b Papillary Thyroid Carcinoma
Il Ku Kang, Kwangsoon Kim, Joonseon Park, Ja Seong Bae, Jeong Soo Kim
Cancers.2022; 14(15): 3677. CrossRef
Characterization of the CpG island methylator phenotype subclass in papillary thyroid carcinoma
Pengfei Gu, Yu Zeng, Weike Ma, Wei Zhang, Yu Liu, Fengli Guo, Xianhui Ruan, Jiadong Chi, Xiangqian Zheng, Ming Gao
Frontiers in Endocrinology.2022;[Epub] CrossRef
MicroRNA Profile for Diagnostic and Prognostic Biomarkers in Thyroid Cancer
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Cancers.2021; 13(4): 632. CrossRef
Lactate Dehydrogenase A as a Potential New Biomarker for Thyroid Cancer
Eun Jeong Ban, Daham Kim, Jin Kyong Kim, Sang-Wook Kang, Jandee Lee, Jong Ju Jeong, Kee-Hyun Nam, Woong Youn Chung, Kunhong Kim
Endocrinology and Metabolism.2021; 36(1): 96. CrossRef
Male sex is not an independent risk factor for recurrence of differentiated thyroid cancer: a propensity score-matching study
Joonseon Park, Kwangsoon Kim, Dong-Jun Lim, Ja Seong Bae, Jeong Soo Kim
Scientific Reports.2021;[Epub] CrossRef
A Newly Developed Pancreatic Adenocarcinoma in a Patient with Advanced Thyroid Cancer under Long-Term Sorafenib Use
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International Journal of Thyroidology.2021; 14(2): 175. CrossRef
Modified risk stratification based on cervical lymph node metastases following lobectomy for papillary thyroid carcinoma
Eyun Song, Jonghwa Ahn, Dong Eun Song, Won Woong Kim, Min Ji Jeon, Tae‐Yon Sung, Tae Yong Kim, Ki Wook Chung, Won Bae Kim, Young Kee Shong, Suck Joon Hong, Yu‐Mi Lee, Won Gu Kim
Clinical Endocrinology.2020; 92(4): 358. CrossRef
Long-term scintigraphic and clinical follow up in patients with differentiated thyroid cancer and iodine avid bone metastases
Omnia Mohamed Talaat, Ismail Mohamed Ali, Sherif Maher Abolyazid, Bader Abdelmaksoud, Ibrahim Mansour Nasr
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Highly prevalent BRAF V600E and low-frequency TERT promoter mutations underlie papillary thyroid carcinoma in Koreans
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Clinical Implication of World Health Organization Classification in Patients with Follicular Thyroid Carcinoma in South Korea: A Multicenter Cohort Study
Meihua Jin, Eun Sook Kim, Bo Hyun Kim, Hee Kyung Kim, Hyon-Seung Yi, Min Ji Jeon, Tae Yong Kim, Ho-Cheol Kang, Won Bae Kim, Young Kee Shong, Mijin Kim, Won Gu Kim
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The age threshold of the 8th edition AJCC classification is useful for indicating patients with aggressive papillary thyroid cancer in clinical practice
Krzysztof Kaliszewski, Dorota Diakowska, Łukasz Nowak, Beata Wojtczak, Jerzy Rudnicki
BMC Cancer.2020;[Epub] CrossRef
Lobectomy Is Feasible for 1–4 cm Papillary Thyroid Carcinomas: A 10-Year Propensity Score Matched-Pair Analysis on Recurrence
Eyun Song, Minkyu Han, Hye-Seon Oh, Won Woong Kim, Min Ji Jeon, Yu-Mi Lee, Tae Yong Kim, Ki Wook Chung, Won Bae Kim, Young Kee Shong, Suck Joon Hong, Tae-Yon Sung, Won Gu Kim
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The binary presence or absence of lymph node metastasis or extrathyroidal extension is not associated with survival in papillary thyroid cancers: Implications for staging systems
Hyun-Soo Zhang, Eun-Kyung Lee, Yuh-Seog Jung, Byung-Ho Nam, Boyoung Park
Cancer Epidemiology.2019; 63: 101589. CrossRef
Risk of Adverse Obstetric Outcomes and the Abnormal Growth of Offspring in Women with a History of Thyroid Cancer
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Changes in Serum Thyroglobulin Levels After Lobectomy in Patients with Low-Risk Papillary Thyroid Cancer
Suyeon Park, Min Ji Jeon, Hye-Seon Oh, Yu-Mi Lee, Tae-Yon Sung, Minkyu Han, Ji Min Han, Tae Yong Kim, Ki-Wook Chung, Won Bae Kim, Young Kee Shong, Won Gu Kim
Thyroid.2018; 28(8): 997. CrossRef
Clinical Outcomes of Differentiated Thyroid Cancer Patients with Local Recurrence or Distant Metastasis Detected in Old Age
Ji Min Han, Ji Cheol Bae, Hye In Kim, Sam Kwon, Min Ji Jeon, Won Gu Kim, Tae Yong Kim, Young Kee Shong, Won Bae Kim
Endocrinology and Metabolism.2018; 33(4): 459. CrossRef
Prognosis of Differentiated Thyroid Carcinoma with Initial Distant Metastasis: A Multicenter Study in Korea
Hosu Kim, Hye In Kim, Sun Wook Kim, Jaehoon Jung, Min Ji Jeon, Won Gu Kim, Tae Yong Kim, Hee Kyung Kim, Ho-Cheol Kang, Ji Min Han, Yoon Young Cho, Tae Hyuk Kim, Jae Hoon Chung
Endocrinology and Metabolism.2018; 33(2): 287. CrossRef
Decreasing Disease-Specific Mortality of Differentiated Thyroid Cancer in Korea: A Multicenter Cohort Study
Min Ji Jeon, Hee Kyung Kim, Eun Heui Kim, Eun Sook Kim, Hyon-Seung Yi, Tae Yong Kim, Ho-Cheol Kang, Young Kee Shong, Won Bae Kim, Bo Hyun Kim, Won Gu Kim
Thyroid.2018; 28(9): 1121. CrossRef
Active Surveillance of Low-Risk Papillary Thyroid Microcarcinoma: A Multi-Center Cohort Study in Korea
Hye-Seon Oh, Jeonghoon Ha, Hye In Kim, Tae Hyuk Kim, Won Gu Kim, Dong-Jun Lim, Tae Yong Kim, Sun Wook Kim, Won Bae Kim, Young Kee Shong, Jae Hoon Chung, Jung Hwan Baek
Thyroid.2018; 28(12): 1587. CrossRef

Clinical Study
Association of the Preoperative Neutrophil-to-ymphocyte Count Ratio and Platelet-to-Lymphocyte Count Ratio with Clinicopathological Characteristics in Patients with Papillary Thyroid Cancer: Sang Mi Kim, Eun Heui Kim, Bo Hyun Kim, Jong Ho Kim, Su Bin Park, Yoon Jeong Nam, Kang Hee Ahn, Min Young Oh, Won Jin Kim, Yun Kyung Jeon, Sang Soo Kim, Yong Ki Kim, In Ju Kim; Endocrinol Metab. 2015;30(4):494-501. Published online December 31, 2015; DOI: https://doi.org/10.3803/EnM.2015.30.4.494

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Background

Several inflammatory biomarkers, especially a high preoperative neutrophil-to-lymphocyte count ratio (NLR) and platelet-to-lymphocyte count ratio (PLR), are known to be indicator of poor prognosis in several cancers. However, very few studies have evaluated the significance of the NLR and PLR in papillary thyroid cancer (PTC). We evaluated the association of the preoperative NLR and PLR with clinicopathological characteristics in patients with PTC.

Methods

This study included 1,066 female patients who underwent total thyroidectomy for PTC. Patients were stratified into 4 quartiles by preoperative NLR and PLR. And the combination of preoperative NLR and PLR was calculated on the basis of data obtained value of tertile as follows: patients with both an elevated PLR and an elevated NLR were allocated a score of 2, and patients showing one or neither were allocated a score of 1 or 0, respectively.

Results

The preoperative NLR and PLR were significantly lower in patients aged ≥45 years and in patients with Hashimoto's thyroiditis. The PLR was significantly higher in patients with tumor size >1 cm (P=0.021).When the patients were categorized into the aforementioned four groups, the group with the higher preoperative PLR was found to have a significantly increased incidence of lateral lymph node metastasis (LNM) (P=0.018). However, there are no significant association between the combination of preoperative NLR and PLR and prognostic factors in PTC patients.

Conclusion

These results suggest that a preoperative high PLR were significant associated with lateral LNM in female patients with PTC.

Citations

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