Abstract
Background:
Mutually increased risks for thyroid and breast cancer have been reported, but the contribution of etiologic factors versus increased medical surveillance to these associations is unknown.
Methods:
Leveraging large-scale US population-based cancer registry data, we used standardized incidence ratios (SIRs) to investigate the reciprocal risks of thyroid and breast cancers among adult females diagnosed with a first primary invasive, non-metastatic breast cancer (N=652,627) or papillary thyroid cancer (PTC) (N=92,318) during 2000–2017 who survived ≥1-year.
Results:
PTC risk was increased 1.3-fold [N=1,434; SIR=1.32; 95% confidence interval (CI)=1.25–1.39] after breast cancer compared to the general population. PTC risk declined significantly with time since breast cancer (Poisson regression=Ptrend <0.001) and was evident only for tumors ≤2 cm in size. The SIRs for PTC were higher after hormone-receptor (HR)+ (versus HR-) and stage II or III (versus stage 0-I) breast tumors. Breast cancer risk was increased 1.2-fold (N=2,038; SIR=1.21; CI=1.16–1.26) after PTC and was constant over time since PTC but was only increased for stage 0-II and HR+ breast cancers.
Conclusion:
Although some of the patterns by latency, stage and size are consistent with heightened surveillance contributing to the breast-thyroid association, we cannot exclude a role of shared etiology or treatment effects.
1. Introduction
A number of studies have reported increased risk for thyroid cancer among breast cancer survivors and the reciprocal increased risk for breast cancer among thyroid cancer survivors.1,2 Past studies have hypothesized that the association between breast and thyroid cancers may be explained by shared etiological factors (e.g., genetic factors [PTEN-mutation] and obesity) or treatment received for initial cancer.1–3 Additionally, cancer survivors undergo heightened clinical surveillance, which may result in incidental detection of primarily early-stage, small-sized tumors that may not have become clinically apparent during the patient’s lifetime.4,5 While it is established that this more intensive clinical surveillance immediately after diagnosis can result in spuriously inflated risks of subsequent malignancies compared with the general population,4 prolonged heightened surveillance also has been suggested as a potential explanation for the observed increased risks of these second breast and thyroid cancers.1,3,6 However, previous studies have not systematically assessed breast and thyroid cancer risks by latency, stage, and tumor size.
2. Methods
2.1. Data and study population
To better understand the potential influence of surveillance versus etiologic factors, including treatment for first primary cancer, on the reciprocal risks of breast and thyroid cancer, we leveraged large-scale, systematically-collected, population-based data from 17 Surveillance, Epidemiology and End Results (SEER) program cancer registries, covering ~28% of the US population.7 We included adult females (20–84 years) who were diagnosed with a first primary invasive, non-metastatic breast cancer (N=652,627) or microscopically-confirmed papillary thyroid cancer (PTC, which accounted for 91.2% of all first primary thyroid cancer cases; N=92,318) during 2000–2017 and survived ≥1 years. The age (<85) and survival (1+ year) restrictions were implemented recognizing potential under-ascertainment of second cancers at older ages and over-ascertainment shortly after initial cancer diagnosis. Additional information ascertained from the registries included race, initial treatment with radiotherapy and/or chemotherapy, and breast cancer hormone receptor (HR) status (Table-1).
Table 1.
Patient characteristics of ≥1-year adult (20–84 years) female survivors of invasive, non-metastatic breast cancer and papillary thyroid cancer, 2000–2017*
| Type of initial cancer |
|||||
|---|---|---|---|---|---|
| First primary breast cancer† |
First primary papillary thyroid cancer† |
||||
| Breast cancer subtypes‡ |
|||||
| Total 652,627 n (%) | HR+ 504,800 | HR− 111,124 | HRunk 36,703 % | Total 92,318 n (%) | |
|
|
|
||||
| Characteristic | n (%) | % | % | % | n (%) |
| Age at diagnosis, y | |||||
| <50 | 167,405 (26) | 24 | 32 | 26 | 53,350 (58) |
| 50–59 | 174,754 (27) | 26 | 30 | 25 | 21,035 (23) |
| 60+ | 310,468 (48) | 50 | 38 | 49 | 17,933 (19) |
| Mean age at diagnosis, y | 59.1 | 59.7 | 56.3 | 59.8 | 47.5 |
| Race | |||||
| White | 526,785 (81) | 82 | 74 | 82 | 75,325 (82) |
| Black | 69,211 (11) | 9 | 18 | 12 | 6,449 (7) |
| Other§ | 56,631 (9) | 9 | 8 | 7 | 10,544 (11) |
| First primary BC stage || | |||||
| 0-I | 328,034 (50) | 53 | 37 | 51 | |
| II | 240,598 (37) | 35 | 45 | 36 | — |
| III | 83,995 (13) | 12 | 18 | 13 | |
| First primary PTC stage ¶ | |||||
| Localized | — | 67,859 (74) | |||
| Regional | 24,459 (26) | ||||
| Latency, y | |||||
| <3 | 652,627 (100) | 100 | 100 | 100 | 92,318 (100) |
| 3-<5 | 514,042 (79) | 79 | 75 | 86 | 75,031 (81) |
| ≥5 | 397,273 (61) | 61 | 58 | 74 | 58,906 (64) |
| Mean follow-up time, y # | 6.3 | 6.1 | 6.1 | 8.5 | 6.5 |
| Any CT/RT | |||||
| CT & no-unk RT | 115,028 (18) | 15 | 30 | 14 | 46 (0) |
| RT & no-unk CT | 188,546 (29) | 34 | 10 | 21 | 42,619 (46) ** |
| CT & RT | 171,558 (26) | 24 | 43 | 15 | 89 (0) |
| no-unk CT & no-unk RT | 177,495 (27) | 28 | 17 | 51 | 49,564 (54) |
Abbreviations: BC, breast cancer; CT, chemotherapy; HR+, hormone receptor positive; HR-, hormone receptor negative; HRunk, hormone receptor unknown; PTC, papillary thyroid cancer; RT, radiation therapy; SEER, surveillance, epidemiology and end results; unk, unknown; y, years
Data derive from 17 US population-based cancer registries of SEER program. See Supplementary Table-1-footnotes (available online) for full details.
First primary invasive BC and PTC cases ascertained using International Classification of Diseases for Oncology, Third Edition (ICD-O-3) morphology and topography codes. PTC cases (restricted to microscopically confirmed cases): topography code - C73.9, and histology codes-8050, 8260, 8340–8344, 8350, 8450–8460. BC cases: topography codes- C500-C509.
BC classified based on the expression of two tumor markers, estrogen receptor (ER), and progesterone receptor (PR): hormone receptor (HR) positive, HR+ (ER+ or borderline [any PR status], PR+ or borderline [any ER status]); HR- (ER- and PR-); HR unknown (all other combinations).
Other race include American Indian or Asian/Pacific Islanders; survivors with unknown race excluded.
First primary BC stage: Stage-6th edition, Breast-Adjusted AJCC 6th Stage (1988–2015) and Stage-7th edition, Derived SEER-Combined Stage Group (2016+).
First primary PTC stage: Summary stage 2000 (1998+); localized (single or multifocal invasive tumor confined to thyroid) or regional (tumor extended beyond thyroid gland).
Patients followed beginning 12 months after initial cancer diagnosis until the first of: second cancer diagnosis, age 85, death, last follow-up, or end of study (December 31, 2017).
Nearly 96% of these 42,708 PTC patients received radioactive iodine towards their radiation therapy.
2.2. Statistical analysis
For the present analyses, patients were followed beginning 12 months after initial cancer diagnosis until the first of: second cancer diagnosis (including in situ breast tumors for analyses of breast cancer following PTC), death, age 85, last follow-up, or end of study (December 31, 2017). Standardized incidence ratios (SIR) and accompanying exact 95% confidence intervals (CI, SEER*Stat v. 8.3.8) quantified the incidence of second primary cancer compared with the general SEER population (see Table-2 footnotes for additional methods). To examine the role of heightened clinical surveillance in the breast-thyroid relationship, we calculated SIRs by stage at diagnosis of the second cancers, tumor size (second PTC-only), and time since first cancer diagnosis (latency). We further investigated risks by breast cancer HR status and type of initial treatment received for first primary breast cancer (chemotherapy and/or radiotherapy) and PTC (radiotherapy) to examine the contribution of these factors on the association between breast cancer and PTC. We used different categories for treatment for the two first primary cancer types because, so few PTC patients received chemotherapy. Likelihood ratio tests derived from multivariable Poisson regression analyses8 were used to evaluate differences (two-sided P<.05) in SIRs by tumor stage, size, latency, initial treatment and HR status of breast cancer using the Amfit module of Epicure.9
Table 2.
Risk of second primary malignancy, bystage and/or size of second cancer, overall and by interval since first cancer diagnosis, among ≥1-year adult (20–84 years) female survivors of invasive, non-metastatic breast cancer and papillary thyroid cancer, 2000–2017*
| Overall |
Latency, y |
||||||||
|---|---|---|---|---|---|---|---|---|---|
| 1-<3 | 3-<5 | 5+ | |||||||
|
|
|||||||||
| O | SIR† (95% CI) | O | SIR†(95% CI) | O | SIR† (95% CI) | O | SIR† (95% CI) | Ptrend‡ | |
| BC → PTC risk § | |||||||||
|
| |||||||||
| Total | 1,434 | 1.32 (1.25 to 1.39) | 530 | 1.82 (1.67 to 1.98) | 295 | 1.24 (1.10 to 1.39) | 609 | 1.10 (1.01 to 1.19) | < 0.001 |
| Stage at second PTC || | |||||||||
| Localized | 1,064 | 1.34 (1.26 to 1.42) | 390 | 1.82 (1.65 to 2.01) | 227 | 1.30 (1.14 to 1.48) | 447 | 1.10 (1.00 to 1.21) | < 0.001 |
| Regional/distant | 353 | 1.29 (1.16 to 1.43) | 137 | 1.87 (1.57 to 2.21) | 64 | 1.07 (0.83 to 1.37) | 152 | 1.08 (0.92 to 1.27) | < 0.001 |
| Unknown/unstaged | 17 | 1.06 (0.62 to 1.70) | 3 | 0.70 (0.14 to 2.03) | 4 | 1.18 (0.32 to 3.03) | 10 | 1.20 (0.58 to 2.21) | > 0.50 |
| Ptrend ¶ | > 0.50 | > 0.50 | 0.178 | > 0.50 | |||||
| Tumor size of second PTC, cm # | |||||||||
| ≤1 | 691 | 1.37 (1.27 to 1.47) | 268 | 2.00 (1.77 to 2.26) | 144 | 1.30 (1.10 to 1.53) | 279 | 1.07 (0.95 to 1.20) | < 0.001 |
| >1 to ≤2 | 431 | 1.46 (1.32 to 1.60) | 170 | 2.14 (1.83 to 2.49) | 74 | 1.14 (0.90 to 1.43) | 187 | 1.24 (1.07 to 1.43) | < 0.001 |
| >2 to ≤4 | 204 | 1.13 (0.98 to 1.29) | 62 | 1.25 (0.96 to 1.60) | 51 | 1.28 (0.95 to 1.68) | 91 | 0.99 (0.80 to 1.22) | 0.130 |
| >4 | 57 | 0.94 (0.71 to 1.22) | 14 | 0.87 (0.48 to 1.46) | 15 | 1.15 (0.64 to 1.90) | 28 | 0.89 (0.59 to 1.28) | > 0.50 |
| Unknown | 51 | 1.21 (0.90 to 1.60) | 16 | 1.27 (0.73 to 2.07) | 11 | 1.18 (0.59 to 2.12) | 24 | 1.19 (0.76 to 1.77) | > 0.50 |
| Ptrend ¶ | 0.002 | < 0.001 | > 0.50 | 0.452 | |||||
|
| |||||||||
| PTC → BC risk § | |||||||||
|
| |||||||||
| Total | 2,038 | 1.21 (1.16 to 1.26) | 523 | 1.25 (1.14 to 1.36) | 413 | 1.16 (1.05 to 1.27) | 1102 | 1.21 (1.14 to 1.28) | > 0.50 |
| Stage at second BC ** | |||||||||
| 0 | 503 | 1.45 (1.33 to 1.58) | 129 | 1.48 (1.24 to 1.76) | 104 | 1.40 (1.15 to 1.70) | 270 | 1.45 (1.28 to 1.64) | > 0.50 |
| I | 788 | 1.22 (1.14 to 1.31) | 194 | 1.24 (1.08 to 1.43) | 161 | 1.20 (1.02 to 1.40) | 433 | 1.23 (1.11 to 1.35) | > 0.50 |
| II | 523 | 1.21 (1.10 to 1.31) | 140 | 1.29 (1.08 to 1.52) | 105 | 1.14 (0.93 to 1.38) | 278 | 1.19 (1.06 to 1.34) | > 0.50 |
| III | 138 | 0.97 (0.82 to 1.15) | 40 | 1.08 (0.77 to 1.47) | 26 | 0.84 (0.55 to 1.24) | 72 | 0.98 (0.76 to 1.23) | > 0.50 |
| IV | 44 | 0.66 (0.48 to 0.88) | 11 | 0.68 (0.34 to 1.22) | 7 | 0.50 (0.20 to 1.03) | 26 | 0.71 (0.46 to 1.04) | > 0.50 |
| Unknown/unstaged | 42 | 0.79 (0.57 to 1.07) | 9 | 0.62 (0.28 to 1.18) | 10 | 0.85 (0.41 to 1.57) | 23 | 0.85 (0.54 to 1.28) | > 0.50 |
| Ptrend ¶ | < 0.001 | 0.009 | < 0.001 | < 0.001 | |||||
Abbreviations: BC, breast cancer; CI, confidence interval; cm, centimeter; O, observed; PTC; papillary thyroid cancer; SEER, surveillance, epidemiology and end results; SIR, standardized incidence ratio; y, years
Data derive from 17 US population-based cancer registries of SEER program. See Supplementary Table-1-footnotes (available online) for full details.
† SIRs: observed-to-expected ratio. Expected number of second primary cancers derived from incidence rates in the total female population of the 17 SEER registries, stratified by age (5-year groups), race (white, black, other) and calendar year (2000–2004, 2005–2009, 2010–2014, 2015–2017), multiplied by appropriate person-years at risk.
Ptrend: Multivariable Poisson regression models adjusted through stratification for age at initial cancer diagnosis (20–39, 40–49, 50–59, 60–69 and 70–84 years) used to conduct two-sided test for trend in SIRs by interval since initial cancer diagnosis (latency; categories modeled as continuous variable) using a likelihood ratio statistic. Inclusion of the log of the expected number of cases as an offset indirectly adjusted for attained age and calendar year, thereby accounting for underlying incidence trends in the general population.
First primary invasive BC and PTC cases ascertained using SEER International Classification of Diseases for Oncology, Third Edition (ICD-O-3) morphology and topography codes. PTC cases: topography code of C73.9 and histology code of 8050, 8260, 8340–8344, 8350, 8450–8460. BC cases: topography codes of C500-C509.
Second primary PTC stage: Summary stage 2000 (1998+)
Ptrend: Multivariable Poisson regression models adjusted through stratification for age at initial cancer diagnosis (20–39, 40–49, 50–59, 60–69 and 70–84 years) and latency (1-<3, 3-<5 and 5+ years) used to conduct two-sided test for trend in SIRs by PTC or BC (as relevant) tumor stage (excluding unknown/unstaged) or tumor size (for PTC only, excluding unknown size) (modeled as continuous variable) using a likelihood ratio statistic. Inclusion of the log of the expected number of cases as an offset indirectly adjusted for attained age and calendar year. Latency adjustment made only in model for the overall group and not for the individual latency groups.
Second primary PTC size: SEER Extent of Disease, Collaborative Staging codes for 2004–2015 and Extent of Disease, Tumor Size Summary (2016+).
Second primary BC stage: Stage-6th edition, Breast-Adjusted AJCC 6th Stage (1988–2015) and Stage-7th edition, Derived SEER-Combined Stage Group (2016+); included both in-situ and invasive disease.
3. Results
3.1. Risk of PTC after breast cancer
For breast cancer survivors, mean age at diagnosis was 59 years, and most women were White (81%) and had HR+ tumors (77%) (Table-1). During a mean of 6.3 years of follow-up, we observed 1,434 PTCs, compared to 1,085 expected in the general population (SIR=1.32; 95%CI=1.25–1.39, Table-2). PTC risks were highest 1-<3 years after breast cancer diagnosis (SIR=1.82; 95%CI=1.67–1.98), declining thereafter (≥5 years: SIR=1.10, 95%CI 1.01–1.19; Ptrend <0.001). SIRs appeared slightly higher for localized PTC, although differences by PTC stage were not statistically significant (Ptrend >0.50). There was, however, significant heterogeneity by PTC size (Ptrend =0.002), with risks significantly higher for smaller tumors (≤2 cm) (SIRs=1.37–1.46) compared to >2cm (SIRs=0.94–1.13). Risk patterns of second PTCs were generally similar for women with HR+ and HR- breast cancer, albeit based on smaller numbers (Supplementary Table-1). Additionally, no significant difference was observed in PTC risk by type of initial treatment (Pheterogeneity=0.097) (Supplementary Table-2) or by PTC variants (classical versus follicular) (data not shown). PTC risk was higher among younger (<50 years) breast cancer survivors, but only during the first 3 years following breast cancer diagnosis. PTC risk varied significantly by stage of first primary breast cancer, with the highest SIRs observed among women diagnosed with a stage III breast cancer (Ptrend <0.001), and this finding remained consistent through all years of follow-up period. The overall pattern of decreasing risk for second PTC with increasing time since breast cancer diagnosis was generally consistent across the patient- and tumor characteristics described above (Table-2, Supplementary Table-1–2).
3.2. Risk of breast cancer after PTC
For PTC survivors, mean age at diagnosis was 47.5 years and most women were White (82%) and had localized disease (74%; Table-1). During a mean of 6.5 years of follow-up, 2,038 in situ (N=503) and invasive (N=1,535) breast cancer cases were diagnosed compared to 1,686 expected in the general population (SIR=1.21; CI=1.16–1.26), with risks remaining elevated ≥5 years after PTC diagnosis (Table-2; Ptrend > 0.50). These stable, elevated risks were observed for stage 0-II second breast cancers, whereas no increased risks were observed overall or at any latency interval for stage III or IV second breast cancers. These patterns were driven exclusively by second HR+ tumors (Supplementary Table-1); no significantly elevated SIRs were observed for HR- tumors after PTC, regardless of stage or latency (Supplementary Table-1). Additionally, BC risk was similar by age at PTC diagnosis, PTC stage (localized versus regional) and radiotherapy (yes versus no/unknown) status (Supplementary Table-2).
4. Discussion
We leveraged large-scale US population-based cancer registry data to examine the association between breast and thyroid cancers by first and second tumor stage (and size for second PTC), latency, breast HR status, and initial treatment received. While we confirm the mutually increased risks reported in previous studies,1,2 we show that the elevated SIRs are largely limited to small, second PTC tumors and localized, HR+ second breast tumors. Additionally, second PTC risks were highest during the first three years following breast cancer diagnosis and among women diagnosed with stage III breast cancer.
Overdiagnosis of both PTC and breast cancer has been extensively discussed in the general literature,10,11 but its role is less-well understood in the context of second cancer risks. In our study, some of the observed risk patterns by latency as well as stage and size of the second cancer for both second PTC and second breast cancer are consistent with heightened clinical surveillance accounting for a portion of the observed increased risk. Specifically, heightened surveillance (i.e., imaging, mammograms, clinical exams, etc.)12–14 among cancer survivors compared with the general population may lead to increased opportunity for incidental detection of second primary tumors that might not otherwise have become clinically apparent. It is unclear whether differences in surveillance patterns by stage at first primary breast cancer diagnosis could also explain the higher SIRs for PTC after later vs earlier stage. Although the risk for second breast cancer after PTC remained elevated for several years after PTC diagnosis, the second breast cancers for which SIRs were elevated (stage 0-I, HR+) are those that are more likely to be incidentally detected.15
Nonetheless, in the absence of individual-level data, we cannot exclude a role of shared genetic, environmental, or treatment-related factors. In particular, we lacked individual-level risk factor information needed to better understand the significantly increased risk for regional/distant stage PTC after breast cancer compared to that observed in the general population. Additional limitations of our study include small numbers of observed cases for analyses stratified by second primary breast cancer HR status, inability to consider other thyroid cancer subtypes, and the relatively short follow-up time. Future studies with detailed patient-level data on hormonal factors (including obesity and use of adjuvant endocrine therapy) as well as surveillance practices following a first primary cancer diagnosis may provide novel insights in the role of shared etiology versus surveillance in the reciprocal risks between breast cancer and PTC. Similarly, studies with detailed treatment-related data (such as radiation fields and doses, specific chemotherapy agents received, etc.) may clarify whether treatment differences underly the observation that subsequent breast cancer risks were largely restricted to HR+ tumors.
5. Conclusion
In conclusion, our analysis of the reciprocal risks for breast and thyroid cancer suggest that the elevated SIRs are largely limited to small, second PTC tumors and localized, HR+ second breast tumors. Future studies with detailed patient-level risk factor data (i.e., hormonal, genetic and treatment factors) as well as information about imaging and other surveillance following the first primary cancer and mode of detection for subsequent malignancies may provide novel insights into the role of etiologic factors versus surveillance in the reciprocal risks between breast cancer and PTC.
Supplementary Material
Acknowledgement
This research was supported by the Intramural Research Program of the National Institutes of Health, National Cancer Institute. The authors acknowledge the efforts of the National Cancer Institute and SEER Program tumor registries in the creation of the SEER database.
Funding
This work was supported by the National Institutes of Health, National Cancer Institute (Z01 CP010131-23 to Dr. Lindsay M Morton).
Footnotes
Conflicts of interest: None
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
References
- 1.Joseph KR, Edirimanne S, Eslick GD. The association between breast cancer and thyroid cancer: a meta-analysis. Breast cancer research and treatment. 2015;152(1):173–181. [DOI] [PubMed] [Google Scholar]
- 2.Nielsen SM, White MG, Hong S, et al. The breast–thyroid cancer link: a systematic review and meta-analysis. Cancer Epidemiology and Prevention Biomarkers. 2016;25(2):231–238. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Schonfeld SJ, Morton LM, de González AB, Curtis RE, Kitahara CM. Risk of second primary papillary thyroid cancer among adult cancer survivors in the United States, 2000–2015. Cancer Epidemiology. 2020;64:101664. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Curtis RE. New malignancies among cancer survivors: SEER cancer registries, 1973–2000. US Department of Health and Human Services, National Institutes of Health; 2006. [Google Scholar]
- 5.Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM. Trends in thyroid cancer incidence and mortality in the United States, 1974–2013. Jama. 2017;317(13):1338–1348. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Bolf EL, Sprague BL, Carr FE. A linkage between thyroid and breast cancer: a common etiology? Cancer Epidemiology and Prevention Biomarkers. 2019;28(4):643–649. [DOI] [PubMed] [Google Scholar]
- 7.Howlader N, Noone A, Krapcho M, et al. SEER Cancer Statistics Review, 1975–2017, National Cancer Institute. Bethesda, MD. 2020. [Google Scholar]
- 8.Yasui Y, Liu Y, Neglia JP, et al. A methodological issue in the analysis of second-primary cancer incidence in long-term survivors of childhood cancers. American journal of epidemiology. 2003;158(11):1108–1113. [DOI] [PubMed] [Google Scholar]
- 9.Preston DL, Lubin JH, Pierce DA, McConney ME, Shilnikova NS. Epicure Risk Regression and Person-Year Computation Software: Command Summary and User Guide. 2015. [Google Scholar]
- 10.Kitahara CM, Sosa JA. The changing incidence of thyroid cancer. Nature Reviews Endocrinology. 2016;12(11):646. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Houssami N. Overdiagnosis of breast cancer in population screening: does it make breast screening worthless? Cancer biology & medicine. 2017;14(1):1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Haugen BR, Alexander EK, Bible KC, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid. 2016;26(1):1–133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Lash TL, Silliman RA. Medical surveillance after breast cancer diagnosis. Medical care. 2001:945–955. [DOI] [PubMed] [Google Scholar]
- 14.Trask PC, Rabin C, Rogers ML, et al. Cancer screening practices among cancer survivors. American journal of preventive medicine. 2005;28(4):351–356. [DOI] [PubMed] [Google Scholar]
- 15.Gaudet MM, Deubler E, Diver WR, et al. Breast cancer risk factors by mode of detection among screened women in the Cancer Prevention Study-II. Breast Cancer Research and Treatment. 2021:1–15. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.