Abstract
Purpose
Our study aimed to assess whether individuals diagnosed with thyroid cancer face an elevated risk of osteoporosis compared to control subjects in a large-scale study. Additionally, we intended to identify potential risk factors associated with osteoporosis in patients with thyroid cancer.
Methods
We used the National Health Insurance Service-National Sample Cohort of South Korea. We included 1,313 patients diagnosed with thyroid cancer and 3,939 control subjects without cancer. Following propensity score matching at a 1:3 ratio, Cox proportional hazards regression and stratification analyses were used to estimate the risk of osteoporosis in patients with thyroid cancer, incorporating multivariate adjustments. A restricted cubic spline model was employed to evaluate dose-response relationships.
Results
Thyroid cancer patients exhibited a higher likelihood of developing osteoporosis than the control group (hazard ratio [HR], 6.59; P < 0.001). In the stratification analyses, younger thyroid cancer patients, females, and those who did not have dyslipidemia were more susceptible to osteoporosis than their counterparts in the control group. Furthermore, the administration of levothyroxine has been linked to an elevated risk of osteoporosis (HR, 2.33; P = 0.044). A restricted cubic spline analysis demonstrated a significant overall association between exposure and outcome (P for total = 0.007, P for nonlinear = 0.573), indicating an essentially linear relationship.
Conclusion
Thyroid cancer patients showed a higher risk of osteoporosis compared to matched controls. Stratified analyses suggested that levothyroxine therapy may be a risk factor for osteoporosis. These findings highlight the importance of individualized treatment approaches.
Keywords: Thyroid neoplasms, Osteoporosis, Levothyroxine
INTRODUCTION
Thyroid cancer is the most prevalent endocrine malignancy, and its occurrence has risen steadily in recent decades [1]. The conventional approach to treating thyroid cancer involves thyroidectomy and levothyroxine therapy, which may lead to imbalances in thyroid hormone levels. This can result in various complications including metabolic syndrome, cardiovascular disease, and osteoporosis [2,3,4,5].
Osteoporosis is a chronic metabolic disorder characterized by reduced bone mass and deterioration of the bone microarchitecture, resulting in an elevated risk of fractures. The pathophysiology of osteoporosis involves an imbalance between bone resorption and formation, which is often influenced by hormonal changes, aging, nutritional deficiencies, and certain medications. While postmenopausal women are at the highest risk owing to estrogen deficiency, other populations, including patients with altered thyroid function, may also be vulnerable [6]. The prevalence of osteoporosis is increasing, imposing a substantial global economic burden on the healthcare system [7]. The escalating healthcare costs and societal impacts highlight the necessity for early diagnosis, preventive strategies, and effective treatment methodologies. Therefore, ongoing research is crucial for developing improved interventions for the prevention and management of osteoporosis [8].
There have still been controversies as to whether thyroid cancer contributes to the incidence of osteoporosis, which is a representative disease caused by bone loss. A recent metaanalysis suggested that postmenopausal women with thyroid cancer had decreased bone mineral density (BMD), while premenopausal women and men did not [9]. Wang et al. reported that levothyroxine treatment for thyroid-stimulating hormone (TSH) suppression induced changes in bone turnover markers, potentially increasing the risk of long-term bone loss [10]. However, several studies reported that levothyroxine treatment did not decrease BMD [11,12,13,14]. These inconsistencies may be explained by heterogeneity of study design or limitations such as small sample sizes and no control.
Therefore, a large-scale study is necessary to investigate whether thyroid cancer is associated with osteoporosis and whether levothyroxine treatment is relevant to osteoporosis. Although a few large-scale studies have suggested an association between levothyroxine treatment and fractures [15,16,17,18], osteoporosis is more tangible with bone health than fracture and occurs in a significantly greater number of cases [19].
We aimed to evaluate whether patients with thyroid cancer exhibit a greater risk of developing osteoporosis than individuals without cancer using a nationwide cohort. We sought to determine the risk factors for osteoporosis in patients with thyroid cancer. Finally, we conducted a nonlinear analysis to assess the correlation between levothyroxine treatment or body mass index (BMI) and risk of osteoporosis.
METHODS
Study population
This study used data from the National Health Insurance Service National Sample Cohort (NSC) database, which included 1,134,108 individuals with information on qualification, health examination results, medical diagnoses (based on International Classification of Diseases, 10th revision [ICD-10]), and prescriptions from January 1, 2002 to December 31, 2019.
We selected prevalent patients who received thyroidectomy after diagnosis of thyroid cancer (ICD-10, C73) from January 1, 2004, to December 31, 2014, and excluded those with a preexisting diagnosis of other cancer (ICD-10, C00-C97, except C73). The control group selection was of individuals who had no diagnosis of malignancies, no thyroidectomy, and no prescription of levothyroxine from January 1, 2002, to December 31, 2019. Then, the thyroid cancer group and the control group were excluded by the following exclusion criteria: (1) previous history of osteoporosis; (2) previous history of other malignancies; (3) age under 19 years or age over 80 years; (4) death or incidence of osteoporosis within 1 year between the cohort entry date and the index date; (5) use of steroid drugs, which could induce osteoporosis more than 3 months before index date; (6) previous history of levothyroxine medication; (7) incomplete information (Fig. 1, Supplementary Fig. 1).
Fig. 1. Flow chart of the study population.
The index date was the 1 year after the cohort entry date. The cohort entry date for thyroid cancer patients was defined as the date of the first prescription of levothyroxine for patients who received levothyroxine treatment, or the date of thyroidectomy for patients who did not receive levothyroxine treatment.
The cohort entry date of the control group was the date of the first health checkup. To address time-related bias, events were censored after a 5-year period from the cohort entry date.
Outcomes and measures
The primary outcome was the incidence of osteoporosis (ICD-10, M80-82). The follow-up period was defined as the time interval between the index date and the date of the study outcome, death, or the end of the study period (December 31, 2019).
Patients with thyroid cancer were further categorized by thyroidectomy type (total thyroidectomy or lobectomy) and whether levothyroxine treatment was administered or not. The average daily dose per weight of levothyroxine (µg/day/kg) was defined as the cumulative levothyroxine dose divided by the total prescription days up to the time of the event and body weight.
Covariates
Demographic characteristics were assessed based on qualification and health examination at the cohort entry date. The residential area was categorized into 2 groups: urban (Seoul, Busan, Daegu, Incheon, Gwangju, Daejeon, and Ulsan) and rural (Gyeonggi Province, Gangwon Province, North and South Chungcheong Provinces, and North and South Jeolla Provinces). Income was categorized into 3 levels: lower, 40%; middle, 30%; and upper 30%. BMI (kg/m2) was categorized into 4 levels: underweight, <18.5; normal, 18.5–22.9; overweight, 23.0–24.9; and obese, ≥25. Smoking status consisted of never, ex-smoker, or current smoker. Heavy drinking was defined as alcohol consumption of more than 7 drinks at least twice per week in males or 5 drinks at least twice per week in females. For participants recruited from 2004 to 2008, regular exercise was defined as at least 5 times per week; after 2009 regular exercise was defined when any 1 of the following 3 criteria were met: vigorous activity at least 3 times per week; mild activity at least 5 times per week; walk at least 5 times per week, based on the International Physical Activity Questionnaire. Dyslipidemia was defined as the use of the ICD-10 code E78 or a total cholesterol level of ≥240 mg/dL. Diabetes was defined as the use of ICD-10 code E10-14 or fasting plasma glucose (FPG) ≥126 mg/dL. Hypertension was defined as the use of ICD-10 codes I10-13 or I15 or blood pressure ≥140/90 mmHg. Charlson Comorbidity Index (CCI) was assessed based on ICD-10 codes (Supplementary Table 1).
Statistical analysis
Descriptive statistics were used to characterize baseline characteristics. Continuous variables are presented as means ± standard deviations. Categorical variables are presented as percentages and absolute numbers. The Student t-test, based on normality, was used to compare continuous variables between the 2 groups, whereas the chi-squared test was used to assess categorical variables. The statistical method of propensity score matching (PSM) was employed to match individuals between the 2 groups in a 1:3 ratio while minimizing the impact of confounding factors. The logistic regression estimated the propensity score model, wherein each subject's estimated probability of being in the thyroid group was based on the given covariates corresponding to the propensity score. In our study, we used age, sex, residential area, insurance type, disability, BMI, heavy drinking, regular exercise, systolic blood pressure (SBP), diastolic blood pressure (DBP), FPG, ALT, AST, total cholesterol, and γ-GT as confounding factors. Caliper was set as 0.02 and greedy nearest neighbor matching was used. Also, a standard mean difference (SMD) of 0.2 was applied to balance between the thyroid cancer group and the control group.
To estimate the hazard ratio (HR) of osteoporosis between the thyroid cancer group and the control group, Cox proportional hazards regression analysis was performed. A Kaplan-Meier curve was obtained to estimate the cumulative incidence of osteoporosis and differences between the 2 groups using the log-rank test. Multivariate analyses were performed using the Cox proportional hazards regression model, which was adjusted for all covariates including age, sex, BMI, smoking status, heavy drinking, regular exercise, income level, SBP, DBP, FPG, ALT, AST, total cholesterol, γ-GT, comorbidities, and CCI. The significant stratified analyses were visualized with a forest plot. To characterize the association of osteoporosis incidence with levothyroxine daily dosage per weight or BMI, levothyroxine daily dosage per weight and BMI were treated as continuous variables and analyzed using restricted cubic spline analysis, with 5 knots located at the 5th, 25th, 50th, 75th, and 95th percentiles of the levothyroxine daily dosage per weight. The reference was 1.53 µg/day/kg of levothyroxine dosage and 23 kg/m2 of BMI.
Preprocessing was conducted using SAS software ver. 9.4 (SAS Institute Inc.). Statistical analyses and visualizations were conducted using R software ver. 4.3.0 (R Foundation for Statistical Computing). Two-sided P-values of <0.05 were considered significant.
Ethics approval
This study was approved by the Institutional Review Board in Konkuk University Medical Center (No. KUMC 2024-08-018) and conducted in accordance with all relevant guidelines and regulations. The requirement for informed consent was not necessary because NSC data were anonymized and researchers could only access them through strict control.
RESULTS
Characteristics of thyroid cancer patients and controls
The total number of participants was 1,313 patients with thyroid cancer and 3,939 matched controls (Table 1). The mean age of the participants was in the mid-40s, and males accounted for about 30%. The follow-up durations were 3.86 years in the thyroid cancer group and 3.55 years in the control group. Baseline characteristics before PSM were presented in Supplementary Table 2.
Table 1. Baseline characteristics of the thyroid cancer group and the control group.
Values are presented as number only, mean ± standard deviation, or number (%).
SMD, standard mean difference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FPG, fasting plasma glucose; TC, total cholesterol.
Among thyroid cancer patients, 78.8% received total thyroidectomy (Supplementary Table 3), 95% received levothyroxine treatment (Supplementary Table 4).
Risk of osteoporosis between patients with thyroid cancer and controls
The risk of osteoporosis showed a significant difference between the thyroid cancer group and the control group (Fig. 2). The HR of thyroid cancer for osteoporosis was 6.59 (95% confidence interval [CI], 2.84–15.28; P < 0.001) compared to the control.
Fig. 2. Cumulative incidence and hazard ratio of osteoporosis in the thyroid cancer group and the control group. The log-rank test showed a significant difference between the 2 groups. PY, person-year; HR, hazard ratio; CI, confidence interval.
Stratification analysis showed that the risk of osteoporosis was significantly higher in the thyroid cancer group than in the control group, regardless of age, heavy drinking, diabetes, hypertension, or CCI (Fig. 3). Females with thyroid cancer showed a higher risk of developing osteoporosis than in the control group (HR, 7.83; 95% CI, 3.18–19.25; P < 0.001). In contrast, males with thyroid cancer demonstrated a statistically insignificant risk of osteoporosis compared to the control group. In addition, there was a significant difference in the incidence of osteoporosis between the thyroid cancer group and the control group when they did not regularly exercise at the the cohort entry date. However, there was no significant difference in the incidence of osteoporosis between the thyroid cancer group and the control group with regular exercise (Fig. 3).
Fig. 3. Stratification analysis of osteoporosis in the thyroid cancer group compared to the control. The forest plot presents the stratification analysis. PY, person-year; HR, hazard ratio; CI, confidence interval; CCI, Charlson Comorbidity Index.
Cox regression and stratification analyses before PSM were presented in Supplementary Fig. 2 and Supplementary Fig. 3.
Effect of thyroidectomy type, levothyroxine treatment, and body mass index on osteoporosis in thyroid cancer patients
Patients who underwent total thyroidectomy showed a higher risk of osteoporosis compared to patients who underwent lobectomy, but the difference was not statistically significant (HR, 1.19; 95% CI, 0.86–1.64; P = 0.305) (Table 2). The levothyroxine treatment group had a significantly higher risk of osteoporosis than the no treatment group (HR, 2.33; 95% CI, 1.02–5.32; P = 0.044) (Table 2).
Table 2. Risk of osteoporosis among patients with thyroid cancer.
Values are presented as number only or number (%).
PY, person-year; HR, hazard ratio; CI, confidence interval.
There was a significant relationship between levothyroxine dosage and risk of osteoporosis (P = 0.007) (Fig. 4A). However, BMI was not significantly associated with the risk of osteoporosis (Fig. 4B).
Fig. 4. Relative risk of osteoporosis in patients with thyroid cancer by levothyroxine dosage and body mass index (BMI). Restricted cubic spline curves characterize the association between levothyroxine dose or BMI (X-axis) and risk of osteoporosis (Y-axis). (A) Daily levothyroxine dose per weight. (B) BMI. The solid line indicates the relative hazard ratio (HR), and the shaded area represents the 95% confidence interval. The reference values are (A) 1.53 µg/day/kg, (B) 23 kg/m2, respectively (HR, 1.0). The spline curve was constructed using 5 knots, specifically placed at (A) 0.9, 1.3, 1.6, 1.9, 2.8 µg/day/kg and (B) 18.8, 21.4, 23.4, 25.6, 29.4 kg/m2.
DISCUSSION
In this nationwide cohort study, we found that patients with thyroid cancer had a significant risk of osteoporosis. It underscored the association between thyroid cancer and bone health. Stratified analyses demonstrated that the association between thyroid cancer and osteoporosis risk differs across age, sex, and dyslipidemia. The increased risk of osteoporosis in the thyroid cancer group was particularly pronounced among younger individuals and females, compared with the control group. It is consistent with previous research suggesting that the incidence of osteoporotic fractures is significantly elevated in thyroid cancer patients aged under 65 years compared to the control group, whereas no significant difference was observed between the 2 groups in individuals aged over 65 years [16]. Furthermore, females with thyroid cancer exhibited a higher incidence of osteoporotic fractures than the control group, while no significant difference was noted in males. These findings suggest that the influence of age and sex on osteoporosis and osteoporotic fractures follows similar patterns [16,17].
Administration of levothyroxine is associated with an increased risk of osteoporosis in patients with thyroid cancer. Therefore, we conducted a restricted cubic spline analysis with the daily levothyroxine dose adjusted for body weight to explore the association between levothyroxine dosage and the risk of osteoporosis. Our findings demonstrate that levothyroxine dosage has a linear relationship with the risk of osteoporosis.
This study had some limitations. First, the database did not provide any information such as BMD, TSH level, or pathological types of thyroid cancer. Osteoporosis is defined as a T score under –2.5 at the axial skeleton by measuring BMD using dual-energy X-ray absorptiometry [20]. However, our study was conducted based on the ICD-10 code, as osteoporosis is usually diagnosed by measuring BMD. Furthermore, we analyzed the osteoporosis association in terms of levothyroxine treatment rather than TSH level. Second, given the observational design of this study, causal inference is precluded. Although we adjusted for multiple potential confounders, the findings should be interpreted as associations rather than evidence of causation. Finally, it would be insufficient to investigate the impact of levothyroxine treatment on the complex relationship between thyroid cancer and risk of osteoporosis, compared to the interaction between other thyroid conditions and the risk of osteoporosis. Further studies are needed to analyze hypothyroid patients as a control group, isolating the effect of levothyroxine therapy more effectively.
Despite these limitations, our study has several strengths. We used a nationwide sample cohort and robust statistical analysis to analyze a more accurate association between thyroid cancer and the risk of osteoporosis in South Korea. We adjusted all covariates including age, sex, BMI, smoking status, heavy drinking, regular exercise, lab measurements, comorbidities, and CCI. Second, we adopted a time-to-event analytic framework rather than a simple cross-sectional comparison of the osteoporosis prevalence. By employing a survival analysis that incorporates censored observations, we precisely characterized both the onset timing and cumulative incidence of osteoporosis. Moreover, the integration of time-varying covariates allows for the rigorous adjustment of confounding factors, thereby enabling a more nuanced assessment of the long-term effects of levothyroxine treatment and substantially enhancing the internal validity of our findings. Finally, the dose-response relationship between levothyroxine and risk of osteoporosis was examined using a restricted cubic spline model. This analysis confirmed a linear association between the daily dosage of levothyroxine and the risk of osteoporosis.
In conclusion, we found that thyroid cancer was associated with a higher risk of osteoporosis than in the control group. Stratification analysis underscored that personalized treatment is necessary, and proper interventions such as physical activity may be beneficial. It also suggested that levothyroxine therapy was associated with an increased risk of osteoporosis in patients with thyroid cancer.
ACKNOWLEDGMENTS
This study used National Health Insurance Service data (NHIS-2024-11-2-016). Due to the National Health Insurance policy restrictions, the original datasets cannot be exported or shared outside the institution. All data generated or analyzed during this study are included in this published article. For further inquiries, please contact the corresponding author.
Footnotes
Fund/Grant Support: This article was supported by the Konkuk University Medical Center.
Conflicts of Interest: No potential conflict of interest relevant to this article was reported.
- Conceptualization, Interpretation: YBC, KSP.
- Statistical analysis, Visualization: YBC.
- Writing – Original Draft: YBC, KSP.
- Writing – Review & Editing: YBC, KSP.
SUPPLEMENTARY MATERIALS
Supplementary Tables 1–4 and Supplementary Figs. 1–3 can be found via https://doi.org/10.4174/astr.2026.110.2.84.
Study design. aComorbidities include hypertension, diabetes, and hyperlipidemia. bFollow-up was censored at the earliest occurrence of death or 5 years from cohort entry date.
Cumulative incidence and hazard ratio of osteoporosis in the thyroid cancer group and the control group before propensity score matching. The log-rank test showed a significant difference between the 2 groups. PY, person-year; HR, hazard ratio; CI, confidence interval.
Stratification analysis of osteoporosis in the thyroid cancer group compared to the control before propensity score matching. The forest plot presents the stratification analysis. PY, person-year.
Definitions of outcome, comorbidities, exposure, and exclusion criteria
Baseline characteristics of thyroid cancer group and control group before propensity score matching
Baseline characteristics in thyroid cancer patients according to thyroidectomy type
Baseline characteristics in thyroid cancer patients according to levothyroxine
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Associated Data
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Supplementary Materials
Study design. aComorbidities include hypertension, diabetes, and hyperlipidemia. bFollow-up was censored at the earliest occurrence of death or 5 years from cohort entry date.
Cumulative incidence and hazard ratio of osteoporosis in the thyroid cancer group and the control group before propensity score matching. The log-rank test showed a significant difference between the 2 groups. PY, person-year; HR, hazard ratio; CI, confidence interval.
Stratification analysis of osteoporosis in the thyroid cancer group compared to the control before propensity score matching. The forest plot presents the stratification analysis. PY, person-year.
Definitions of outcome, comorbidities, exposure, and exclusion criteria
Baseline characteristics of thyroid cancer group and control group before propensity score matching
Baseline characteristics in thyroid cancer patients according to thyroidectomy type
Baseline characteristics in thyroid cancer patients according to levothyroxine