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Long-Term Follow-Up of Thyroid Incidentalomas Visualized with 18F diagnostics Article Long-Term Follow-Up of Thyroid Incidentalomas Visualized with 18F-Fluorodeoxyglucose Positron Emission Tomography—Impact of Thyroid Scintigraphy in the Diagnostic Work-Up Kirsten Korsholm 1,*, Michala Reichkendler 1, Louise Alslev 1, Åse Krogh Rasmussen 2 and Peter Oturai 1 1 Department of Clinical Physiology, Nuclear Medicine and PET, Copenhagen University Hospital, Rigshospitalet, DK-2100 Copenhagen, Denmark; [email protected] (M.R.); [email protected] (L.A.); [email protected] (P.O.) 2 Department of Endocrinology, Copenhagen University Hospital, Rigshospitalet, DK-2100 Copenhagen, Denmark; [email protected] * Correspondence: [email protected] Abstract: Our objective was to evaluate the frequency of malignancy in incidental thyroidal uptake on 18F-fluorodeoxyglucose positron emission tomography/computed tomography (18F-FDG PET/CT) in a cohort of Danish patients, and furthermore to evaluate the impact of thyroid scinti-graphy in the diagnostic work-up. All whole-body PET/CT reports from 1 January 2010 to 31 December 2013 Citation: Korsholm, K.; were retrospectively reviewed and further analyzed if visually increased thyroidal FDG uptake was Reichkendler, M.; Alslev, L.; reported. Patient electronic files were searched for further thyroid evaluation. Of 13,195 18F-FDG- Rasmussen, Å.K.; Oturai, P. PET/CT scans in 9114 patients, 312 PET/CT reports mentioned incidental thyroid FDG-uptake, and Long-Term Follow-Up of Thyroid 279 patients were included in the study (3.1%). The thyroid was further investigated in 137 patients Incidentalomas Visualized with 18F-Fluorodeoxyglucose Positron (49%), and 75 patients underwent thyroid scintigraphy. A total of 57 patients had a thyroid biopsy Emission Tomography—Impact of and 21 proceeded to surgery. Surgical specimens displayed malignancy in 10 cases, and one thyroid Thyroid Scintigraphy in the malignancy was found by autopsy. Hence, 11 patients were diagnosed with thyroid malignancies Diagnostic Work-Up. Diagnostics 2021, among 279 patients with incidental thyroid 18F-FDG uptake (3.9%). In 34 patients, a biopsy was 11, 557. https://doi.org/10.3390/ avoided due to the results of the thyroid scintigraphy. We conclude that patients with thyroid diagnostics11030557 incidentalomas can benefit from further diagnostic work-up including a thyroid scintigraphy. Academic Editor: Christian la Keywords: thyroid; incidentalomas; thyroid malignancy; thyroid scintigraphy; 18F-FDG-PET Fougere Received: 4 March 2021 Accepted: 18 March 2021 1. Introduction Published: 19 March 2021 Incidental thyroid nodules (ITN) are defined as nodules originally detected on ima- Publisher’s Note: MDPI stays neutral ging studies performed in patients with no thyroid-related clinical symptoms, examination with regard to jurisdictional claims in findings, nor suspicion of thyroid disease [1]. Due to the increased use of imaging, more and published maps and institutional affil- more ITN are discovered, as thyroid nodules are common in the general Danish population. iations. Population studies in Denmark have shown that 15% of women in the age group 40 to 45 years have multiple nodules >1 cm in their thyroid gland, and that the prevalence increases to 25–30% in women age 60–65 years [2]; however, in Denmark the incidence of thyroid malignancy is only 360 new cases per year (6.2 cases per 100,000 inhabitants/year) (https://www.dahanca.dk/assets/files/Aar_r_DAHANCA_2018.pdf, accessed on 26 June Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. 2020). In the United States, the incidence of thyroid cancer nearly tripled from 1975 to This article is an open access article 2009, and despite this change in incidence, the mortality rate from thyroid cancer remained distributed under the terms and stable [3]. This is partly explained by over-diagnosing and partly by the fact that small conditions of the Creative Commons thyroid cancers can have an indolent course, and an ideal approach would be only to Attribution (CC BY) license (https:// diagnose those cancers that are likely to be of clinical significance. creativecommons.org/licenses/by/ 18F-Fluorodeoxyglucose positron emission tomography (18F-FDG-PET) visualizes 4.0/). cells with increased glucose demand such as malignantly transformed cells; however, Diagnostics 2021, 11, 557. https://doi.org/10.3390/diagnostics11030557 https://www.mdpi.com/journal/diagnostics Diagnostics 2021, 11, 557 2 of 12 this high glucose uptake is nonspecific and may also represent inflammation, infection or increased glandular activity [4,5]. Large studies and systematic reviews report a prevalence of 1−2.5% of ITNs with increased FDG-uptake in PET scans, with a frequency of malignancy of the ITNs with focal FDG uptake of approximately 33% [6–9]. To discriminate between benign and malignant thyroid tissue, researchers have thoroughly investigated standardized maximum FDG uptake value (SUVmax) of the ITNs. A large meta-analysis of 16 studies [9] reported that 9 studies demonstrated a significant difference between malignant and benign lesions, while the other 7 found no such difference, indicating that there is no safe cut-off value below which malignancy can be ruled out. The American Thyroid Association recommends that patients with focal metabolic activity in the thyroid detected on 18F-FDG-PET scans undergo dedicated thyroid ultra- sonography and fine-needle aspiration cytology (FNAC) if there is a solid lesion ≥1 cm corresponding to the FDG-avid lesion [10]. However, unless the cytology result is defini- tively benign or malignant, patients may undergo repeated biopsies or diagnostic surgery. Hoang et al. reported that 25−41% of patients who undergo FNAC for ITNs will proceed to surgery, and 36−75% of these patients will have benign nodules [11]. The context of underlying disease and life expectancy should therefore be kept in mind when further investigations are initiated [12]. In Denmark, a thyroid scintigraphy is a common part of the evaluation of thyroid nodules, and a Danish study suggested that patients with ITN detected by 18F-FDG-PET should undergo thyroid scintigraphy and ultrasonography followed by FNAC if a nodule is hypo-functioning [13]. In our center, approximately 6000 whole-body 18F-FDG-PET scans are performed yearly (2016–2019). If an FDG-positive ITN is detected, the patient may be referred for further diagnostic procedures, usually including a thyroid scintigraphy and ultrasonography. We find it of interest to investigate the frequency of FDG-avid ITNs in Eastern Denmark, the frequency of malignant lesions, and the thyroid scintigraphy findings in patients with FDG- avid lesions in the thyroid. As scintigraphically hyperfunctioning nodules have a very low risk of malignancy [14], unnecessary biopsies and surgery might be prevented when using a thyroid scintigraphy in the diagnostic work-up. To our knowledge, only one other study has addressed the combined use of thyroid scintigraphy and FDG-PET to detect possible malignant lesions in the thyroid [15], however, no study has investigated the impact of thyroid scintigraphy in the diagnostic work-up of FDG-avid ITNs in a large cohort of patients. 2. Materials and Methods 2.1. Patients From 1 January 2010 to 31 December 2013, 13,195 whole-body 18F-FDG-PET/CT scans were performed in the Department of Clinical Physiology, Nuclear Medicine, and PET, Copenhagen University Hospital, Rigshospitalet, in 9114 patients. Of these, 312 scans reported increased FDG uptake in the thyroid gland. All 312 scan reports were individually reviewed, resulting in 279 patients included in the study. Patients were excluded if they had known or suspected malignant thyroid disease, or if they had a previous 18F-FDG-PET/CT scan, where increased thyroid FDG uptake was reported. In addition, 18F-FDG-PET/CT scans performed for radiation therapy planning or scans performed in research protocols were excluded. All medical files were searched, and the clinical decisions upon the results of the 18F-FDG-PET/CT report were scrutinized. Data concerning thyroid scintigraphy, thyroid ultrasonography, plasma-stimulating thyroid hormone (P-TSH), FNACs, coarse needle biopsies, pathological examination of surgical specimens, clinical follow-up, and date of eventual death were sampled. In addition, all patients were searched in The Danish Pathology Data Bank (a database containing results of all Danish pathological examinations). The main part of the patients came from Eastern Denmark. Diagnostics 2021, 11, 557 3 of 12 2.2. PET Imaging The PET/CT images were obtained using Biograph mCT-S (64–128 slices) and Bio- graph TrueV (40–64 slices) scanners (Siemens Medical Solutions, Malvern, PA, USA) and a Discovery LS (16 slices) scanner (GE Healthcare, Waukesha, WI, USA). The patients were intravenously injected with 4 MBq/kg 18F-FDG after a minimum of 6 hours of fasting, and the PET/CT was performed approximately 60 min after tracer injection. The CT scan was performed as diagnostic CT with contrast-enhancement or low-dose CT without contrast. Images were originally interpreted by a team consisting of a nuclear medicine physi- cian and a radiologist, and pathological FDG-uptake was reported when detected. Sub- sequently, 18F-FDG-PET scans of patients included in the study were re-evaluated, and pathological FDG uptake in the thyroid was classified as either focal, multifocal, or diffuse; maximum standardized uptake value (SUVmax) was obtained for the FDG-avid areas. All the ITNs were mentioned in
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