Endocrinology and Metabolism

Volume 38(3); June 2023

Review Articles

Thyroid
Diagnosis and Management of Thyroid Disease during Pregnancy and Postpartum: 2023 Revised Korean Thyroid Association Guidelines: Hwa Young Ahn, Ka Hee Yi; Endocrinol Metab. 2023;38(3):289-294. Published online June 9, 2023; DOI: https://doi.org/10.3803/EnM.2023.1696

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Thyroid hormone plays a critical role in fetal growth and development, and thyroid dysfunction during pregnancy is associated with several adverse outcomes, such as miscarriage and preterm birth. In this review, we introduce and explain three major changes in the revised Korean Thyroid Association (KTA) guidelines for the diagnosis and management of thyroid disease during pregnancy: first, the normal range of thyroid-stimulating hormone (TSH) during pregnancy; second, the treatment of subclinical hypothyroidism; and third, the management of euthyroid pregnant women with positive thyroid autoantibodies. The revised KTA guidelines adopt 4.0 mIU/L as the upper limit of TSH in the first trimester. A TSH level between 4.0 and 10.0 mIU/L, combined with free thyroxine (T4) within the normal range, is defined as subclinical hypothyroidism, and a TSH level over 10 mIU/L is defined as overt hypothyroidism regardless of the free T4 level. Levothyroxine treatment is recommended when the TSH level is higher than 4 mIU/L in subclinical hypothyroidism, regardless of thyroid peroxidase antibody positivity. However, thyroid hormone therapy to prevent miscarriage is not recommended in thyroid autoantibody-positive women with normal thyroid function.

Citations

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Use of thyroid hormones in hypothyroid and euthyroid patients: A survey of members of the Endocrine Society of Australia
Nicole Lafontaine, Suzanne J. Brown, Petros Perros, Enrico Papini, Endre V. Nagy, Roberto Attanasio, Laszlo Hegedüs, John P. Walsh
Clinical Endocrinology.2024; 100(5): 477. CrossRef
A Prospective Clinical Trial of Radiofrequency Ablation in Patients with Low-Risk Unifocal Papillary Thyroid Microcarcinoma Favoring Active Surveillance Over Surgery
Ji Ye Lee, Dong Gyu Na, Jung Suk Sim, Jin Yong Sung, Sun Wook Cho, Do Joon Park, Young Joo Park, Ji-hoon Kim
Thyroid®.2024; 34(9): 1126. CrossRef
Association between antinuclear antibodies status and preterm birth in Japanese pregnant women: a prospective cohort study from Adjunct Study of the Japan Environment and Children’s Study
Mami Fukushige, Xi Lu, Minoru Satoh, Masako Oda, Takashi Ohba, Takahiko Katoh
BMC Pregnancy and Childbirth.2024;[Epub] CrossRef
Management of Subclinical Hypothyroidism: A Focus on Proven Health Effects in the 2023 Korean Thyroid Association Guidelines
Eu Jeong Ku, Won Sang Yoo, Hyun Kyung Chung
Endocrinology and Metabolism.2023; 38(4): 381. CrossRef
Maternal isolated hypothyroxinemia in the first trimester is not associated with adverse pregnancy outcomes, except for macrosomia: a prospective cohort study in China
Jing Du, Linong Ji, Xiaomei Zhang, Ning Yuan, Jianbin Sun, Dan Zhao
Frontiers in Endocrinology.2023;[Epub] CrossRef

Calcium & bone metabolism
Skeletal Senescence with Aging and Type 2 Diabetes: Joshua Nicholas Farr; Endocrinol Metab. 2023;38(3):295-301. Published online June 14, 2023; DOI: https://doi.org/10.3803/EnM.2023.1727

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Osteoporosis and type 2 diabetes (T2D) are common diseases that often coexist. While both of these diseases are associated with poor bone quality and increased fracture risk, their pathogenesis of increased fracture risk differs and is multifactorial. Mounting evidence now indicates that key fundamental mechanisms that are central to both aging and energy metabolism exist. Importantly, these mechanisms represent potentially modifiable therapeutic targets for interventions that could prevent or alleviate multiple complications of osteoporosis and T2D, including poor bone quality. One such mechanism that has gained increasing momentum is senescence, which is a cell fate that contributes to multiple chronic diseases. Accumulating evidence has established that numerous boneresident cell types become susceptible to cellular senescence with old age. Recent work also demonstrates that T2D causes the premature accumulation of senescent osteocytes during young adulthood, at least in mice, although it remains to be seen which other bone-resident cell types become senescent with T2D. Given that therapeutically removing senescent cells can alleviate age-related bone loss and T2D-induced metabolic dysfunction, it will be important in future studies to rigorously test whether interventions that eliminate senescent cells can also alleviate skeletal dysfunction in context of T2D, as it does with aging.

Citations

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AGEs (Advanced Glycation End-products) in bone come of age
Deepak Vashishth, Ruban Dhaliwal, Mishaela Rubin
Bone.2025; 190: 117301. CrossRef
Single-cell sequencing reveals an important role of SPP1 and microglial activation in age-related macular degeneration
Shizhen Lei, Mang Hu, Zhongtao Wei
Frontiers in Cellular Neuroscience.2024;[Epub] CrossRef
The synergistic effect of diabetes mellitus and osteoporosis on the all-cause mortality: a cohort study of an American population
Weihua Li, Siyu Xie, Shengdong Zhong, Liting Lan
Frontiers in Endocrinology.2024;[Epub] CrossRef
Identification of systemic biomarkers and potential drug targets for age-related macular degeneration
Shizhen Lei, Mang Hu, Zhongtao Wei
Frontiers in Aging Neuroscience.2024;[Epub] CrossRef
Senescence-related genes and proteins in the development of Alzheimer’s disease: evidence from transcriptomic and Mendelian randomization analysis
Ying Liu, Jiao Chen
Frontiers in Aging Neuroscience.2024;[Epub] CrossRef

Editorial

Diabetes, obesity and metabolism
Cardiovascular Risk Reduction in Type 2 Diabetes: Further Insights into the Power of Weight Loss and Exercise: Seung-Hwan Lee; Endocrinol Metab. 2023;38(3):302-304. Published online June 28, 2023; DOI: https://doi.org/10.3803/EnM.2023.1751

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Original Articles

Diabetes, obesity and metabolism
Effects of Weight Loss and Interaction with Physical Activity on Risks of Cardiovascular Outcomes in Individuals with Type 2 Diabetes: Claudia R. L. Cardoso, Nathalie C. Leite, Gil F. Salles; Endocrinol Metab. 2023;38(3):305-314. Published online May 31, 2023; DOI: https://doi.org/10.3803/EnM.2023.1690

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Background
This study investigated the effects of weight loss during follow-up on cardiovascular outcomes in a type 2 diabetes cohort and tested interactions with clinical and laboratory variables, particularly physical activity, that could impact the associations.
Methods
Relative weight changes were assessed in 651 individuals with type 2 diabetes and categorized as ≥5% loss, <5% loss, or gain. Associations between weight loss categories and incident cardiovascular outcomes (total cardiovascular events [CVEs], major adverse cardiovascular events [MACEs], and cardiovascular mortality) were assessed using multivariable Cox regression with interaction analyses.
Results
During the initial 2 years, 125 individuals (19.2%) lost ≥5% of their weight, 180 (27.6%) lost <5%, and 346 (53.1%) gained weight. Over a median additional follow-up of 9.3 years, 188 patients had CVEs (150 MACEs) and 106 patients died from cardiovascular causes. Patients with ≥5% weight loss had a significantly lower risk of total CVEs (hazard ratio [HR], 0.52; 95% confidence interval, 0.33 to 0.89; P=0.011) than those who gained weight, but non-significant lower risks of MACEs or cardiovascular deaths. Patients with <5% weight loss had risks similar to those with weight gain. There were interactions between weight loss and physical activity. In active individuals, ≥5% weight loss was associated with significantly lower risks for total CVEs (HR, 0.20; P=0.004) and MACEs (HR, 0.21; P=0.010), whereas in sedentary individuals, no cardiovascular protective effect of weight loss was evidenced.
Conclusion
Weight loss ≥5% may be beneficial for cardiovascular disease prevention, particularly when achieved with regular physical activity, even in high-risk individuals with long-standing type 2 diabetes.

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Weight change in patients with new‐onset type 2 diabetes mellitus and its association with remission: Comprehensive real‐world data
Jinyoung Kim, Bongseong Kim, Mee Kyoung Kim, Ki‐Hyun Baek, Ki‐Ho Song, Kyungdo Han, Hyuk‐Sang Kwon
Diabetes, Obesity and Metabolism.2024; 26(2): 567. CrossRef
Body weight variability and the risk of liver‐related outcomes in type 2 diabetes and steatotic liver disease: a cohort study
Nathalie C. Leite, Claudia R. L. Cardoso, Cristiane A. Villela‐Nogueira, Gil F. Salles
Obesity.2024; 32(6): 1210. CrossRef
Cardiovascular Risk Reduction in Type 2 Diabetes: Further Insights into the Power of Weight Loss and Exercise
Seung-Hwan Lee
Endocrinology and Metabolism.2023; 38(3): 302. CrossRef
Effects of body weight variability on risks of macro- and microvascular outcomes in individuals with type 2 diabetes: The Rio de Janeiro type 2 diabetes cohort
Claudia R.L. Cardoso, Nathalie C. Leite, Gil F. Salles
Diabetes Research and Clinical Practice.2023; 205: 110992. CrossRef

Diabetes, obesity and metabolism
Association between Serum Amyloid A Levels and Type 2 Diabetes Mellitus: A Systematic Review and Meta-Analysis: Ting Liu, Meng Li, Chunying Cui, Jielin Zhou; Endocrinol Metab. 2023;38(3):315-327. Published online June 7, 2023; DOI: https://doi.org/10.3803/EnM.2023.1621

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Background
To date, consistent data have not been reported on the association between serum amyloid A (SAA) levels and type 2 diabetes mellitus (T2DM). The purpose of this study was to systematically summarize their relationship.
Methods
Databases including PubMed, Cochrane Library, Embase, Web of Science, and MEDLINE were searched until August 2021. Cross-sectional and case-control studies were included.
Results
Twenty-one studies with 1,780 cases and 2,070 controls were identified. SAA levels were significantly higher in T2DM patients than in healthy groups (standardized mean difference [SMD], 0.68; 95% confidence interval [CI], 0.39 to 0.98). A subgroup analysis showed that the mean age of participants and the continent that participants were from were related to differences in SAA levels between cases and controls. Furthermore, in T2DM patients, SAA levels were positively associated with body mass index (r=0.34; 95% CI, 0.03 to 0.66), triglycerides (r=0.12; 95% CI, 0.01 to 0.24), fasting plasma glucose (r=0.26; 95% CI, 0.07 to 0.45), hemoglobin A1c (r=0.24; 95% CI, 0.16 to 0.33), homeostasis model assessment for insulin resistance (r=0.22; 95% CI, 0.10 to 0.34), C-reactive protein (r=0.77; 95% CI, 0.62 to 0.91), and interleukin-6 (r=0.42; 95% CI, 0.31 to 0.54), but negatively linked with highdensity lipoprotein cholesterol (r=–0.23; 95% CI, –0.44 to –0.03).
Conclusion
The meta-analysis suggests that high SAA levels may be associated with the presence of T2DM, as well as lipid metabolism homeostasis and the inflammatory response.

Citations

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Correlation between insulin resistance and the rate of neutrophils-lymphocytes, monocytes-lymphocytes, platelets-lymphocytes in type 2 diabetic patients
Yuanyuan Zhang, Huaizhen Liu
BMC Endocrine Disorders.2024;[Epub] CrossRef
Integrated Network-Based Analysis of Diseases Associated with Amyloid Deposition Through a Disease–Protein–Drug Network
Aikaterini E. I. Rizou, Georgia I. Nasi, Avgi E. Apostolakou, Meletios A. Dimopoulos, Efstathios Kastritis, Vassiliki A. Iconomidou
Pharmaceuticals.2024; 17(12): 1736. CrossRef
Antioxidant and Anti-Inflammatory Functions of High-Density Lipoprotein in Type 1 and Type 2 Diabetes
Damien Denimal
Antioxidants.2023; 13(1): 57. CrossRef

Diabetes, obesity and metabolism
Efficacy of Gemigliptin Add-on to Dapagliflozin and Metformin in Type 2 Diabetes Patients: A Randomized, Double-Blind, Placebo-Controlled Study (SOLUTION): Byung Wan Lee, KyungWan Min, Eun-Gyoung Hong, Bon Jeong Ku, Jun Goo Kang, Suk Chon, Won-Young Lee, Mi Kyoung Park, Jae Hyeon Kim, Sang Yong Kim, Keeho Song, Soon Jib Yoo; Endocrinol Metab. 2023;38(3):328-337. Published online June 28, 2023; DOI: https://doi.org/10.3803/EnM.2023.1688

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Background
This study evaluated the efficacy and safety of add-on gemigliptin in patients with type 2 diabetes mellitus (T2DM) who had inadequate glycemic control with metformin and dapagliflozin.
Methods
In this randomized, placebo-controlled, parallel-group, double-blind, phase III study, 315 patients were randomized to receive either gemigliptin 50 mg (n=159) or placebo (n=156) with metformin and dapagliflozin for 24 weeks. After the 24-week treatment, patients who received the placebo were switched to gemigliptin, and all patients were treated with gemigliptin for an additional 28 weeks.
Results
The baseline characteristics were similar between the two groups, except for body mass index. At week 24, the least squares mean difference (standard error) in hemoglobin A1c (HbA1c) changes was –0.66% (0.07) with a 95% confidence interval of –0.80% to –0.52%, demonstrating superior HbA1c reduction in the gemigliptin group. After week 24, the HbA1c level significantly decreased in the placebo group as gemigliptin was administered, whereas the efficacy of HbA1c reduction was maintained up to week 52 in the gemigliptin group. The safety profiles were similar: the incidence rates of treatment-emergent adverse events up to week 24 were 27.67% and 29.22% in the gemigliptin and placebo groups, respectively. The safety profiles after week 24 were similar to those up to week 24 in both groups, and no new safety findings, including hypoglycemia, were noted.
Conclusion
Add-on gemigliptin was well tolerated, providing comparable safety profiles and superior efficacy in glycemic control over placebo for long-term use in patients with T2DM who had poor glycemic control with metformin and dapagliflozin.

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Dual add‐on therapy of gemigliptin and dapagliflozin in patients with type 2 diabetes inadequately controlled with metformin alone: The SOLUTION 2 study
Kyung Ah Han, You‐Cheol Hwang, Shin Je Moon, Ho Chan Cho, Hye Jin Yoo, Sung Hee Choi, Suk Chon, Kyoung‐Ah Kim, Tae Nyun Kim, Jun Goo Kang, Cheol‐Young Park, Jong Chul Won, Eunjoo Cho, Jeongyun Kim, Kyong Soo Park
Diabetes, Obesity and Metabolism.2024; 26(9): 3743. CrossRef

Thyroid
The Early Changes in Thyroid-Stimulating Immunoglobulin Bioassay over Anti-Thyroid Drug Treatment Could Predict Prognosis of Graves’ Disease: Jin Yu, Han-Sang Baek, Chaiho Jeong, Kwanhoon Jo, Jeongmin Lee, Jeonghoon Ha, Min Hee Kim, Jungmin Lee, Dong-Jun Lim; Endocrinol Metab. 2023;38(3):338-346. Published online June 9, 2023; DOI: https://doi.org/10.3803/EnM.2023.1664

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Background
To determine whether baseline thyroid-stimulating immunoglobulin (TSI) bioassay or its early response upon treatment with an anti-thyroid drug (ATD) can predict prognosis of Graves’ disease (GD) in real-world practice.
Methods
This retrospective study enrolled GD patients who had previous ATD treatment with TSI bioassay checked at baseline and at follow-up from April 2010 to November 2019 in one referral hospital. The study population were divided into two groups: patients who experienced relapse or continued ATD (relapse/persistence), and patients who experienced no relapse after ATD discontinuation (remission). The slope and area under the curve at 1st year (AUC_1yr) of thyroid-stimulating hormone receptor antibodies including TSI bioassay and thyrotropin-binding inhibitory immunoglobulin (TBII) were calculated as differences between baseline and second values divided by time duration (year).
Results
Among enrolled 156 study subjects, 74 (47.4%) had relapse/persistence. Baseline TSI bioassay values did not show significant differences between the two groups. However, the relapse/persistence group showed less decremental TSI bioassay in response to ATD than the remission group (–84.7 [TSI slope, –198.2 to 8.2] vs. –120.1 [TSI slope, –204.4 to –45.9], P=0.026), whereas the TBII slope was not significantly different between the two groups. The relapse/persistence group showed higher AUC_1yr of TSI bioassay and TBII in the 1st year during ATD treatment than the remission group (AUC_1yr for TSI bioassay, P=0.0125; AUC_1yr for TBII, P=0.001).
Conclusion
Early changes in TSI bioassay can better predict prognosis of GD than TBII. Measurement of TSI bioassay at beginning and follow-up could help predict GD prognosis.

Citations

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Enhanced predictive validity of integrative models for refractory hyperthyroidism considering baseline and early therapy characteristics: a prospective cohort study
Xinpan Wang, Tiantian Li, Yue Li, Qiuyi Wang, Yun Cai, Zhixiao Wang, Yun Shi, Tao Yang, Xuqin Zheng
Journal of Translational Medicine.2024;[Epub] CrossRef
Long-term Effect of Thyrotropin-binding Inhibitor Immunoglobulin on Atrial Fibrillation in Euthyroid Patients
Jung-Chi Hsu, Kang-Chih Fan, Ting-Chuan Wang, Shu-Lin Chuang, Ying-Ting Chao, Ting-Tse Lin, Kuan-Chih Huang, Lian-Yu Lin, Lung-Chun Lin
Endocrine Practice.2024; 30(6): 537. CrossRef
Dynamic Risk Model for the Medical Treatment of Graves’ Hyperthyroidism according to Treatment Duration
Meihua Jin, Chae A Kim, Min Ji Jeon, Won Bae Kim, Tae Yong Kim, Won Gu Kim
Endocrinology and Metabolism.2024; 39(4): 579. CrossRef
A Predictive Model for Graves’ Disease Recurrence After Antithyroid Drug Therapy: A Retrospective Multicenter Cohort Study
Omar El Kawkgi, David Toro-Tobon, Freddy J.K. Toloza, Sebastian Vallejo, Cristian Soto Jacome, Ivan N. Ayala, Bryan A. Vallejo, Camila Wenczenovicz, Olivia Tzeng, Horace J. Spencer, Jeff D. Thostenson, Dingfeng Li, Jacob Kohlenberg, Eddy Lincango, Sneha M
Endocrine Practice.2024;[Epub] CrossRef

Thyroid
Thyroid Hormone Reference Intervals among Healthy Individuals In Lanzhou, China: Yan Lu, Wen-Xia Zhang, De-Hong Li, Lian-Hua Wei, Yu-Jun Zhang, Fu-Na Shi, Shen Zhou; Endocrinol Metab. 2023;38(3):347-356. Published online June 14, 2023; DOI: https://doi.org/10.3803/EnM.2023.1638

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Background
The common reference intervals (RIs) for thyroid hormones currently used in China are provided by equipment manufacturers. This study aimed to establish thyroid hormone RIs in the population of Lanzhou, a city in the subplateau region of northwest China, and compare them with previous reports and manufacturer-provided values.
Methods
In total, 3,123 individuals (1,680 men, 1,443 women) from Lanzhou, an iodine-adequate area of China, perceived as healthy were selected. The Abbott Architect analyzer was used to determine the serum concentration of thyroid hormones. The 95% RI was estimated using the 2.5th and 97.5th percentiles as the lower and upper reference limits, respectively.
Results
The serum levels of thyroid-stimulating hormone (TSH), total triiodothyronine (TT3), antithyroglobulin (ATG) antibody, and antithyroid peroxidase (ATPO) antibody levels were significantly correlated with sex (P<0.05). TSH, total thyroxine (TT4), and ATPO levels were significantly correlated with age (P<0.05). The serum levels of TSH, ATG, and ATPO in men were significantly lower than in women; in contrast, the serum TT3 level was significantly higher in men than in women (P<0.05). Serum TSH, TT3, TT4, and ATG levels differed across age groups (P<0.05), but no such variation was observed for ATG levels (P>0.05). The established RIs of TSH, ATG, and ATPO in this study differed between sexes (P<0.05). The thyroid hormone RIs established herein were inconsistent with the manufacturer-provided values.
Conclusion
The RIs of thyroid hormones in the healthy population of Lanzhou were inconsistent with those in the manufacturer’s manual. Validated sex-specific values are required for diagnosing thyroid diseases.

Citations

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Burden of non-alcoholic fatty liver disease in subclinical hypothyroidism
Mahmood Dhahir Al-Mendalawi
Journal of Clinical and Scientific Research.2024; 13(1): 68. CrossRef

Corrigendum

Thyroid
Corrigendum: Abstract and Text Correction. Thyroid Stimulating Hormone Reference Range and Prevalence of Thyroid Dysfunction in the Korean Population: Korea National Health and Nutrition Examination Survey 2013 to 2015: Won Gu Kim, Won Bae Kim, Gyeongji Woo, Hyejin Kim, Yumi Cho, Tae Yong Kim, Sun Wook Kim, Myung-Hee Shin, Jin Woo Park, Hai-Lin Park, Kyungwon Oh, Jae Hoon Chung; Endocrinol Metab. 2023;38(3):357. Published online May 16, 2023; DOI: https://doi.org/10.3803/EnM.2023.301; Corrects: Endocrinol Metab 2017;32(1):106

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