This cross-sectional study assesses the association of sociodemographic factors with the odds of receiving a biopsy, timeliness of the procedure, and risk of nodule malignancy.
Key Points
Question
Are sociodemographic disparities associated with the diagnostic management of pediatric thyroid nodules?
Findings
In this cross-sectional study of 11 643 children with thyroid nodules, greater parental education was associated with a shorter diagnosis-to-biopsy interval among children who received a biopsy. There were no gender or racial differences in the odds of nodule malignant neoplasm, though female gender, older age, and White race were associated with greater odds of receiving a biopsy.
Meaning
The findings highlight disparities in the timeliness of biopsy of pediatric thyroid nodules, but no sociodemographic differences were associated with risk of malignant neoplasm among biopsied nodules.
Abstract
Importance
Thyroid cancer is the most common pediatric endocrine malignant neoplasm. Disparities in the workup of thyroid nodules may be significantly associated with thyroid cancer outcomes.
Objective
To determine the association of sociodemographic factors with the odds of receiving a biopsy, timeliness of the procedure, and risk of nodule malignancy.
Design, Setting, and Participants
This was a retrospective cross-sectional study using insurance claims data from the Optum Clinformatics Data Mart database. The study cohort comprised pediatric patients diagnosed with single thyroid nodules between 2003 and 2020. Data analysis was performed from January 1, 2003, to June 30, 2020.
Main Outcomes and Measures
Multivariable logistic regression models were used to identify demographic variables associated with biopsy and nodule malignant neoplasm. A multivariable linear regression model was used to assess the time between thyroid nodule diagnosis and biopsy.
Results
Of 11 643 children (median [IQR] age at diagnosis or procedure, 15 [12-17] years; 8549 [73.2%] were female and 3126 [26.8%] were male) diagnosed with single thyroid nodules, 2117 (18.2%) received a biopsy. Among the patients who received a biopsy, 304 (14.4%) were found to have a malignant nodule. Greater parental education was associated with a shorter diagnosis-to-biopsy interval (mean difference, −7.24 days; 95% CI, −13.75 to −0.73). Older age at nodule diagnosis (odds ratio [OR], 1.11; 95% CI, 1.09-1.13) and female gender (OR, 1.25; 95% CI, 1.11-1.40) were associated with increased odds of receiving a biopsy, while Black/African American (OR, 0.80; 95% CI, 0.65-0.99) and Hispanic (OR, 0.84; 95% CI, 0.72-0.99) patients had lower odds of receiving a biopsy compared with White patients. Finally, female gender (OR, 1.08; 95% CI, 0.80-1.47) was not associated with lower odds of nodule malignant neoplasm.
Conclusions and Relevance
Findings of this cross-sectional study highlight disparities in the diagnostic management of pediatric thyroid nodules. These results call for future work to ensure equitable access to thyroid care for all children.
Introduction
Differentiated thyroid cancer is the most common pediatric endocrine malignant neoplasm,1 and its incidence has been increasing.2,3 In adults, social disparities in thyroid cancer care have been associated with worse overall and disease-specific morbidity and mortality,4,5,6 and similar disparities have been identified in children.7,8,9 While prior work has focused on care after the diagnosis of thyroid cancer, identifying upstream social disparities during the workup of pediatric thyroid nodules may be useful for improving overall outcomes.
Ultrasound-guided biopsy is considered the standard of care for the evaluation of thyroid nodules in children,10 as it is diagnostic and influences subsequent management of thyroid nodules. Here, we use insurance claims data from a single commercial insurer to identify 11 643 children diagnosed with single thyroid nodules between January 2003 and June 2020. The goals of this study were to assess the association of sociodemographic factors with the odds of receiving a biopsy and the timeliness of this procedure and to identify factors associated with a higher risk of nodule malignancy. The use of insurance data is a novel approach to study thyroid nodules. While this strategy focuses on the subset of the US population with commercial insurance and excludes uninsured or publicly insured individuals, it controls for the effect of insurance type and allows for the identification of social disparities in pediatric thyroid health care access independently of insurance type.
Methods
Data Source
A retrospective analysis of insurance claims data was conducted using Optum’s Clinformatics Data Mart database (OptumInsight) from January 1, 2003, to June 30, 2020. This source contains deidentified claims data from a commercial insurer that accounts for approximately 12 million unique patients annually from all 50 US states and territories, of which 24% are children. Optum data compare favorably with data from the 2010 US Census with respect to the following demographic factors: gender, age, race and ethnicity (in Optum, race or ethnicity of participants were selected by parents of the following categories: White [non-Hispanic], Black/African American, Hispanic, Asian, and other), and geographic region (eTable in the Supplement).11 These data are publicly available to researchers for a fee per year of data. As this data source is deidentified, our study was exempt from review by the Stanford University institutional review board. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline.
Study Design
We included patients with diagnoses of a single thyroid nodule (International Classification of Diseases, Ninth Revision [ICD-9]: 241.0, 246.2; International Statistical Classification of Diseases and Related Health Problems, Tenth Revision [ICD-10]: E04.1) at age 18 years or younger and those who received an ultrasound-guided fine-needle aspiration or core biopsy (Current Procedural Terminology: 10021-2, 10025-6, 60100, 76942), and identified those who subsequently were diagnosed with thyroid malignant neoplasm (ICD-9: 193; ICD-10: C73). Patients diagnosed with multiple nodules (ie, ICD-9: 241.1—nontoxic multinodular goiter) were excluded from the study. Information on sonographic features of nodules (ie, size, echogenicity, margin) is not available in the database, as there are no insurance codes that correspond to ultrasonography findings. Among children who received a biopsy, the time interval between the date of thyroid nodule diagnosis and the date of biopsy was calculated. Sociodemographic information, including age at diagnoses, gender, race and ethnicity, and highest attained education of the primary policyholder, was obtained from the database.
Statistical Analyses
Statistical analyses were performed using Stata, version 16.1 (StataCorp LLC). Descriptive statistics were used to report the percentage of children receiving biopsies and the incidence of differentiated thyroid carcinoma among children with thyroid nodules. Among all children, multivariable logistic regression was used to identify demographic variables that were associated with receiving a biopsy. Then among those biopsies, multivariable linear regression was used to predict the number of days between thyroid nodule diagnosis and biopsy, and a multivariable logistic regression model was used to predict odds of thyroid carcinoma. Effect sizes were reported as adjusted odds ratios (ORs) and adjusted mean difference for multivariable logistic and linear regressions, respectively, with accompanying 95% CIs.
Results
In total, 11 643 children (median [IQR] age at diagnosis or procedure, 15 [12-17] years; 8549 [73.2%] were female and 3126 [26.8%] were male) were diagnosed with single thyroid nodules, and 2117 (18.2%) received a biopsy. Among patients who received a biopsy, 304 (14.4%) had concurrent or subsequent diagnoses of thyroid malignant neoplasm. Adolescents, females, and people of White race accounted for the majority of the study cohort. Detailed sociodemographic characteristics are summarized in Table 1. Proportions of children by age are shown in the Figure.
Table 1. Characteristics of Children With Diagnoses of Solitary Thyroid Nodules and Subcohorts Who Received Ultrasound-Guided Biopsies and Received Diagnoses of Thyroid Neoplasm.
| Characteristic | No. (%) | ||
|---|---|---|---|
| Thyroid nodule diagnosis (n = 11 643) | Ultrasound-guided biopsy (n = 2117) | Thyroid malignant neoplasm diagnosis (n = 304) | |
| Age at diagnosis or procedure, median (IQR), y | 15 (12-17) | 16 (14-17) | 16 (14-17) |
| Gender | |||
| Female | 8549 (73.2) | 1671 (78.9) | 243 (79.9) |
| Male | 3126 (26.8) | 446 (21.1) | 61 (20.1) |
| Race and ethnicity | |||
| Asian | 505 (4.3) | 84 (4.0) | 15 (4.9) |
| Black/African American | 712 (6.1) | 118 (5.6) | 17 (5.6) |
| Hispanic | 1292 (11.1) | 212 (10.0) | 36 (11.8) |
| White | 7308 (62.6) | 1436 (67.8) | 198 (65.1) |
| Other/unknowna | 1858 (15.9) | 267 (12.6) | 38 (12.5) |
| Parental education | |||
| <Bachelor’s | 7511 (64.3) | 1383 (65.3) | 198 (65.1) |
| ≥Bachelor’s | 2650 (22.7) | 519 (24.5) | 76 (25.0) |
| Unknown | 1514 (13.0) | 215 (10.2) | 30 (9.9) |
“Other” was its own category in the Optum database. Missing data were categorized as “unknown.” These categories were combined for statistical analyses.
Figure. Proportion of Children Who Received Thyroid Nodule Diagnosis, Ultrasound-Guided Biopsy, and Thyroid Malignant Neoplasm Diagnosis by Age.
Multiple logistic regression was used to identify factors associated with receiving a biopsy among all children suspected of having thyroid nodules accounting for age at nodule diagnosis, gender, race and ethnicity, and parental education (Table 2). Older age at nodule diagnosis was significantly associated with increased odds of receiving a biopsy (OR, 1.11; 95% CI, 1.09-1.13), as was female gender (OR, 1.25; 95% CI, 1.11-1.40). Compared with White patients, Black/African American (OR, 0.80; 95% CI, 0.65-0.99) and Hispanic (OR, 0.84; 95% CI, 0.72-0.99) patients had significantly lower odds of receiving a biopsy. Higher parental education trended toward increased odds of receiving a biopsy (OR, 1.10; 95% CI, 0.98-1.24).
Table 2. Results of Logistic Regression Predicting Odds of Receiving an Ultrasound-Guided Biopsy Among All Children Diagnosed With a Thyroid Nodule (n = 11 643 With Thyroid Nodules; n = 2117 Who Received FNA).
| Variable | Adjusted OR (95% CI) |
|---|---|
| Age at nodule diagnosis, per year | 1.11 (1.09-1.13) |
| Gender | |
| Female | 1.25 (1.11-1.40) |
| Male | 1 [Reference] |
| Race and ethnicity | |
| Asian | 0.89 (0.69-1.13) |
| Black/African American | 0.80 (0.65-0.99) |
| Hispanic | 0.84 (0.72-0.99) |
| White | 1 [Reference] |
| Other/unknown | 0.76 (0.58-1.00) |
| Parental education | |
| <Bachelor’s | 1 [Reference] |
| ≥Bachelor’s | 1.10 (0.98-1.24) |
| Unknown | 0.96 (0.71-1.29) |
Abbreviations: FNA, fine-needle aspiration; OR, odds ratio.
Among children who received biopsies, the median (IQR) time between initial thyroid nodule diagnosis and biopsy was 29 (4-229) days. Multivariable linear regression was performed to assess whether age at nodule diagnosis, gender, race and ethnicity, and parental education were associated with the time interval between nodule diagnosis and biopsy (Table 3). After adjusting for all variables, parental education level of a bachelor’s degree or higher was associated with a significantly shorter interval by 1 week (mean difference, −7.24 days; 95% CI, −13.75 to −0.73 days). No other variables were associated with time to biopsy.
Table 3. Results of Linear Regression Predicting Mean Difference (MD) in Days Between Date of Thyroid Nodule Diagnosis and Ultrasound-Guided Biopsy (n = 2117).
| Variable | Adjusted MD (95% CI), d |
|---|---|
| Age at nodule diagnosis, per year | −0.06 (−0.99 to 0.86) |
| Gender | |
| Female | −2.25 (−8.92 to 4.41) |
| Male | 1 [Reference] |
| Race and ethnicity | |
| Asian | −12.23 (−26.84 to 2.37) |
| Black/African American | −2.31 (−13.82 to 9.20) |
| Hispanic | 3.96 (−5.50 to 13.42) |
| White | 1 [Reference] |
| Other/unknown | −7.93 (−23.30 to 7.43) |
| Parental education | |
| <Bachelor’s | 1 [Reference] |
| ≥Bachelor’s | −7.24 (−13.75 to −0.73) |
| Unknown | 12.27 (−4.61 to 29.14) |
It is historically thought that among children with thyroid nodules, males are more likely to have a thyroid malignant neoplasm.12,13 We performed a multiple logistic regression among children who received a biopsy, accounting for demographic characteristics including age at nodule diagnosis, gender, and race and ethnicity (Table 4). In the cohort, we found that females did not have significantly different odds of having a thyroid malignant neoplasm than males (OR, 1.08; 95% CI, 0.80-1.47). Additionally, age at nodule diagnosis and race and ethnicity were not associated with odds of thyroid malignant neoplasm.
Table 4. Results of Logistic Regression Predicting Odds of Thyroid Malignant Neoplasm Among Children Who Received a Biopsy (n = 2117 With Biopsy; n = 304 With Thyroid Malignant Neoplasm).
| Variable | Adjusted OR (95% CI) |
|---|---|
| Age at nodule diagnosis, per year | 1.00 (0.96-1.04) |
| Gender | |
| Female | 1.08 (0.80-1.47) |
| Male | 1 [Reference] |
| Race and ethnicity | |
| Asian | 1.36 (0.76-2.42) |
| Black/African American | 1.05 (0.62-1.80) |
| Hispanic | 1.28 (0.87-1.89) |
| White | 1 [Reference] |
| Other/unknown | 1.04 (0.71-1.51) |
Abbreviation: OR, odds ratio.
Discussion
The primary objective of this study was to assess for disparities in the diagnostic workup for pediatric thyroid nodules. The results show that among children who received a biopsy, greater parental education was associated with a shorter diagnosis-to-biopsy interval. Female gender, older age, and White race were associated with greater odds of receiving a biopsy. Reassuringly, there were no differences in the odds of receiving fine-needle aspiration by education status, and there were no differences in the odds of nodule malignant neoplasm based on race and ethnicity or education.
To our knowledge, this study is the first to systematically assess for sociodemographic disparities in the diagnostic workup of pediatric thyroid nodules. Prior studies have described downstream disparities in pediatric thyroid cancer care after diagnosis, such as in clinical presentation, survival, costs, and timeliness of care. Sosa et al8 reported that children from lower-income families were more likely to have complications from surgery, longer inpatient stays, and higher costs. The authors also described racial and ethnic disparities in access to high-volume surgeons. Garner et al7 found that lower income and lack of insurance were associated with treatment delay and more advanced cancer at presentation. Recently, Gruszczynski et al9 reported that individuals from racial and ethnic minority groups and males were at higher risk for presenting with more advanced disease and worse survival compared with non-Hispanic White individuals and females, respectively. Given that ultrasound-guided biopsy is necessary to evaluate thyroid nodules for malignant neoplasm, investigating disparities in the use of this diagnostic modality may help explain previously reported disparities in overall outcomes.
In terms of time to biopsy, higher education level of the primary policyholder was the only factor associated with shorter interval time. As education level is often considered a proxy for socioeconomic status14 and/or health literacy,15 our results are consistent with previous work that has described the association of these factors with the timeliness of receiving care.16,17,18 Mean difference in time to biopsy was small, and in isolation, the disparity may not have a clinically significant association with overall outcomes. However, this finding could be a reflection of variation in health care utilization patterns between families of differing backgrounds and may be compounded onto other phases of disease management, including time interval to treatment.7,18 To validate this extrapolation, future studies should investigate whether delays in the diagnostic management of pediatric thyroid cancer correlate with differences in disease stage at presentation and treatment outcomes. In addition, it is important to note that the differences in time to biopsy were detectable despite this cohort being uniformly insured by a single commercial insurer. Inclusion of publicly insured patients may have revealed starker differences that may have clinical importance. Future studies on cohorts with greater heterogeneity in health coverage may capture disparities in the timeliness of care that are more representative of the general population.
The study also showed that no sociodemographic factors were associated with higher risk of nodule malignancy. While it is traditionally thought that nodules found in males have a higher probability of malignancy,12,13 the present study is not the first to report that gender was not associated with differences in malignancy risk. In their retrospective review of 314 pediatric patients, Richman et al19 analyzed sonographic and demographic characteristics of thyroid nodules and found no gender difference in the likelihood of malignant neoplasm. Similarly, Gupta et al20 analyzed nodules in 300 patients and found that gender was not significantly associated with cancer risk. Racial differences in malignancy risk of nodules have previously been described in adult patients. Zheng et al21 demonstrated that Black/African American race was associated with lower rates of thyroid malignant neoplasm in thyroid nodules compared with other races and ethnicities. To our knowledge, differences in thyroid malignancy risk in thyroid nodules have not been previously reported in children. In the current study cohort, we found no association between race and ethnicity and nodule malignant neoplasm. It should be noted that prior studies reporting on overall risk factors for pediatric thyroid malignant neoplasm within a population identified Hispanic race and ethnicity as a risk factor.22 It is possible that Hispanic children are at higher overall risk for thyroid malignant neoplasm due to a higher prevalence of thyroid nodules and/or potentially increased rates of autoimmune thyroiditis,23 though individual nodules in this population have equal probability of malignancy compared with those in people of other races and ethnicities. Future work is necessary to further elucidate how rates of thyroid nodules and thyroid malignant neoplasms differ between sociodemographic groups.
Among children with suspected thyroid nodules, female gender, older age, and White race were associated with higher odds of receiving a biopsy. These findings are reflective of the overall increased incidence and prevalence of pediatric thyroid cancer by these demographic variables.2,24,25,26 Given that no sociodemographic factors were associated with higher malignancy risk once a biopsy was performed, this finding suggests that biopsies were ordered equitably in this commercially insured cohort.
In the present study, 63% of the children with single thyroid nodules were White, compared with the 53% reported for Optum’s overall database population. We would expect to observe a similar race distribution between the groups if there was no association between race and detection or development of thyroid nodules. This prompts the question of whether White children are more likely to develop thyroid nodules relative to their counterparts of other races and ethnicities. If so, this is a crucial and explanatory finding given that White children have higher incidence rates of thyroid cancer. Researchers have long speculated whether racial differences in incidence rates are due to differences in access to care or factors such as genetic predisposition or environmental exposures.22 For example, maternal education, often used as a proxy for socioeconomic status and health care access,22,27 is highest among White individuals28 and is associated with greater odds of a child being diagnosed with thyroid cancer.22 In terms of genetic risk factors, several studies have used molecular diagnostics to profile pediatric thyroid nodules and have identified key gene fusions and sequence variations that are common in children who develop malignant neoplasm.29,30 Investigators did not find differences by race but were limited by sample size, and therefore this question remains the subject of future research. Finally, there is some evidence suggesting that non-Hispanic White children are more likely to be exposed to certain environmental pollutants, such as polychlorinated biphenyls,31 which has been implicated as a risk factor for thyroid cancer.32,33 Ultimately, it is unknown whether the 10% gap in the proportion of White children in the present study cohort and the Optum population represents a true difference given the level of missingness in race and ethnicity data of the Optum database (approximately 25%). We did not perform statistical analysis such as a 2-proportions z test, as it would not have yielded a meaningful result given the large sample size of each group. Future work is still needed to delineate if White race is a true risk factor for thyroid nodules and, in turn, cancer.
Limitations
This study has several limitations. As with all studies using administrative claims, the results are contingent on the specificity and accuracy of medical coding, as well as the accuracy of the sociodemographic variables. We chose specific ICD codes to define our inclusion criteria, thereby increasing the internal validity of the study. Consequently, the cohort does not reflect children with nontoxic multinodular goiter who might have undergone biopsy of a dominant nodule, limiting the generalizability of the results. Notably, information on sonographic features of biopsied thyroid nodules was not available in claims data. Future studies can provide a more nuanced understanding of whether “high-risk” nodules in the different sociodemographic groups are being preferentially biopsied in accordance with the American Thyroid Association guidelines.10 In addition, we only included the first biopsy, though some patients may have had repeated biopsies if initial results were inconclusive. Exclusion of this data may not have a significant effect, as literature reports that up to 90% of patients only require 1 round of biopsy.20,34 Furthermore, we defined a single biopsy variable regardless of procedure type and assumed that the average patient had similar access to fine-needle aspiration and core biopsy. Finally, the cohort represents patients from a single commercial insurer, which is both a strength and weakness of this study. By standardizing insurance within the cohort, we were able to assess differences in health care use independently of insurance type. However, these results may not be representative of the general population, where disparities may be amplified.
Conclusions
To our knowledge, this cross-sectional study is the first to systematically assess for sociodemographic disparities in the diagnostic management of pediatric thyroid nodules. Greater parental education was associated with a shorter interval between nodule diagnosis and ultrasound-guided biopsy. Several factors were associated with greater odds of receiving a biopsy, including female gender, older age, and White race. Among biopsied nodules, there were no sociodemographic differences in the risk for thyroid malignant neoplasm. These results describe social disparities in management of pediatric thyroid nodules and call for future work to ensure equitable access to thyroid care for all children.
eTable. Demographic characteristics by proportion
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Supplementary Materials
eTable. Demographic characteristics by proportion
