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Yasuhiro Ito Department of Surgery, Kuma Hospital, Shimoyamate-dori, Chuo-ku, Kobe, Hyogo, Japan

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Akira Miyauchi Department of Surgery, Kuma Hospital, Shimoyamate-dori, Chuo-ku, Kobe, Hyogo, Japan

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Graphical abstract

Abstract

Papillary and follicular thyroid carcinomas (PTC and FTC) are prominent malignancies that originate from thyroid follicular cells. PTC is usually diagnosed via preoperative cytology, and large tumor size, clinical node metastasis, and distant metastasis constitute preoperative prognostic factors. Gross extrathyroidal and extranodal tumor extensions have a significant prognostic impact, are evaluated intraoperatively, and are useful for determining the extent of surgery. Aggressive variants, such as tall cell and hobnail variants, a high Ki-67 labeling index (LI), and somatic gene mutations are prognostic factors in postoperative pathological and molecular examinations. In contrast, FTC is generally diagnosed based on postoperative pathology. Large tumor size and M factors have prognostic value; however, the findings of pathological examinations are very important. FTCs are classified as minimally invasive, encapsulated angioinvasive, and widely invasive FTCs. Widely invasive FTC with vascular invasion (VI) and encapsulated angioinvasive FTCs with extensive VI have a poor prognosis, whereas widely invasive FTC without VI has an excellent prognosis, which is similar to that of minimally invasive FTC. This indicates that VI is a considerably more important prognostic marker than capsular invasion. For postoperative follow-up, dynamic markers such as the thyroglobulin-doubling rate (DR), metastatic tumor volume-DR, and change in the neutrophil-to-lymphocyte ratio are important and are useful for evaluating the effectiveness of treatments, such as radioactive iodine therapy and molecular targeted therapy, for recurrent lesions. For clinicians, it is important to accurately evaluate prognostic markers of PTC and FTC in the pre-, intra-operative, and post-operative phases.

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Hirotoshi Nakamura Kuma Hospital, Kobe, Japan

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Akane Ide Kuma Hospital, Kobe, Japan

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Takumi Kudo Kuma Hospital, Kobe, Japan

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Eijun Nishihara Kuma Hospital, Kobe, Japan

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Mitsuru Ito Kuma Hospital, Kobe, Japan

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Akira Miyauchi Kuma Hospital, Kobe, Japan

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Objective: Finding agranulocytosis (AG) at an early stage is important to improve outcome, but periodic granulocyte count monitoring is not generally recommended for patients with Graves' disease, because AG develops suddenly. Method: At the Kuma Hospital, Graves' patients under antithyroid drug (ATD) treatment in an outpatient clinic have a granulocyte count examination during each visit, and if it is <1,000/μl, a warning is immediately sent to the patient's physician. We evaluated the usefulness of this system. Results: We investigated 25 AG and 33 granulocytopenia (GP) cases over a recent 5-year period, excluding patients who developed AG or GP at another hospital and were referred to us for treatment. Among the 25 AG patients, 16 patients (64%; 9 asymptomatic and 7 very mild symptomatic cases) were discovered by the periodic granulocyte count examination at an outpatient clinic. The remaining 9 patients visited the Kuma Hospital or other hospitals because of infection symptoms. Most of the AG patients were given granulocyte colony-stimulating factor injections immediately and were admitted if a prompt increase in granulocytes could not be obtained. The final treatments for Graves' disease were <sup>131</sup>I-radioisotope therapy (19 patients), thyroidectomy (2 patients), inorganic iodine (1 patient), or another ATD (1 patient). Among the 33 GP patients, 31 (94%), including 20 asymptomatic cases, were discovered during periodic granulocyte count monitoring. Most of them stopped ATD, and other treatments for Graves' disease were selected. Conclusion: Periodic monitoring of granulocyte counts is useful for identifying AG and GP patients with no or minimum infection symptoms.

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Eijun Nishihara Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Nobuyuki Amino Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Takumi Kudo Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Kazuyoshi Kohsaka Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Mitsuru Ito Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Shuji Fukata Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Mitsushige Nishikawa Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Hirotoshi Nakamura Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Akira Miyauchi Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Background: Subacute thyroiditis is generally believed to be induced by viral infection, and little attention has been paid to anti-thyroid antibodies. Objectives: Our study aimed to assess the prevalence of anti-thyroid antibodies in patients with subacute thyroiditis. Methods: Anti-thyroglobulin (TgAb) and anti-thyroid peroxidase antibodies (TPOAb) were measured with 4 different immunoassay kits currently used in 40 patients in the early phase of subacute thyroiditis. Results: The proportion of samples positive for TgAb was 52.5 ± 13.7% (mean of 4 kits), which was significantly (p < 0.05) higher than that positive for TPOAb (15.6 ± 6.5%). The prevalence of positive TgAb alone (negative TPOAb) was also significantly higher than that of TPOAb alone (negative TgAb). TgAb titers decreased or disappeared within 4 months to 6 years in 6 patients. Conclusions: Patient samples were moderately positive for TgAb initially, but the titer decreased or disappeared afterwards in subacute thyroiditis.

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Hirosuke Danno Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Eijun Nishihara Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Kazuyoshi Kousaka Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Tomohiko Nakamura Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Toshihiko Kasahara Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Takumi Kudo Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Mitsuru Ito Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Shuji Fukata Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Mitsushige Nishikawa Division of Internal Medicine, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Akira Miyauchi Division of Surgery and Director, Center for Excellence in Thyroid Care, Kuma Hospital, Kobe, Japan

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Introduction: Marine-Lenhart syndrome (MLS) is now understood to be a combination of Graves’ disease and autonomously functioning thyroid nodule(s) (AFTNs). The prevalence of the syndrome and suitable treatments for those living in iodine-sufficient areas are uncertain. Objectives: We aimed to investigate the prevalence, treatment, and prognosis of MLS in Japan, an iodine-sufficient area. Methods: This study involved patients who visited our hospital between February 2005 and August 2019. Among patients with both thyrotoxicosis and thyroid nodule(s) larger than 10 mm, MLS and isolated AFTNs were diagnosed based on serum thyroid-stimulating hormone receptor antibody levels and scintigraphy using radioiodine or technetium-99m and thyroid uptake. Results: Twenty-two patients were found to have MLS, compared to 372 with isolated AFTNs and 8,343 with Graves’ disease, during the period. Therefore, the rate of MLS cases was 0.26% among all patients with Graves’ disease (22/8,343). Treatments and outcomes were assessed for cases of MLS (n = 18) and isolated AFTNs (n = 269). Antithyroid drugs (ATDs) were withdrawn in 27.8% of cases in the MLS group and 10.3% in the isolated AFTN group. There was no significant difference in the clinical outcome after ATD withdrawal between the 2 groups. However, the rate of hypothyroidism after radioactive iodine (RAI) administration was significantly higher in the MLS group than in the isolated AFTN group (42.9 vs. 9.0%, p = 0.005) despite similar doses of RAI. Conclusions: The prevalence of MLS among patients with Graves’ disease was 0.26% in Japan. RAI therapy induces hypothyroidism more frequently than in those with AFTNs probably because RAI is taken up in the surrounding Graves’ tissues.

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Kaoru Kobayashi Kuma Hospital, Kobe City, Hyogo, Japan

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Mitsuyoshi Hirokawa Kuma Hospital, Kobe City, Hyogo, Japan

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Tomonori Yabuta Kuma Hospital, Kobe City, Hyogo, Japan

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Mitsuhiro Fukushima Kuma Hospital, Kobe City, Hyogo, Japan

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Minoru Kihara Kuma Hospital, Kobe City, Hyogo, Japan

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Yuuki Takamura Kuma Hospital, Kobe City, Hyogo, Japan

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Yasuhiro Ito Kuma Hospital, Kobe City, Hyogo, Japan

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Akihiro Miya Kuma Hospital, Kobe City, Hyogo, Japan

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Nobuyuki Amino Kuma Hospital, Kobe City, Hyogo, Japan

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Akira Miyauchi Kuma Hospital, Kobe City, Hyogo, Japan

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Background: Thyroid nodules with cystic content or mixed sponge-like aspect on ultrasonography and a concordant cytology are strongly predictive of benignity. Objectives: We present 8 patients with honeycomb-like papillary thyroid carcinoma with multiple small cysts on ultrasonography. Methods: The patients were 6 women and 2 men aged between 30 and 57 years. The tumors of these patients showed honeycomb-like multiple small cysts that were aggregated in some area of the thyroid gland on ultrasonography. Histopathological examination indicated a well-differentiated type of papillary thyroid carcinoma with multiple small cysts and a small solid lesion. The cysts were lined with papillary carcinoma cells, and normal thyroid tissue lay between the cysts. Results: There is a peculiar type of papillary thyroid carcinoma that histopathologically shows honeycomb-like multiple small cysts in the thyroid gland. Ultrasonography can be used to identify characteristic features of honeycomb-like multiple small cysts in the thyroid gland in such patients. Conclusions: One should be aware of this peculiar type of papillary thyroid carcinoma with honeycomb-like multiple small cysts on ultrasonography, although thyroid nodules with cystic lesions are generally regarded as benign in clinical management.

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Eijun Nishihara Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Yoshitaka Hobo ASKA Pharmamedical Co., Ltd. Fujisawa, Japan

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Akira Miyauchi Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Yasuhiro Ito Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Miyoko Higuchi Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Mitsuyoshi Hirokawa Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Mitsuru Ito Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Shuji Fukata Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Mitsushige Nishikawa Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Takashi Akamizu Kuma Hospital, Center for Excellence in Thyroid Care, Kobe, Japan

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Objective

This study aimed to elucidate disproportionately low serum thyroglobulin (Tg) values in Tg antibody (TgAb)-positive patients with structural recurrence of papillary thyroid carcinoma (PTC) using liquid chromatography-tandem mass spectrometry (LC-MS/MS).

Design

A retrospective study was performed on 176 patients in whom Tg and TgAb levels were measured between 2016 and 2021. Several comprehensive analyses of Tg-LC-MS/MS with an electrochemiluminescence immunoassay for Tg (Tg-ECLIA) were conducted using serum samples.

Methods

TgAb-positive patients who underwent total thyroidectomy with multiple lung metastases due to PTC were evaluated using Tg-LC-MS/MS and Tg-ECLIA. Tg expression in lymph node metastases and metastatic lesions was evaluated by immunohistochemistry and Tg levels of aspiration washouts were also evaluated. Two in vitro assays were performed to elucidate TgAb interference.

Results

Tg concentrations of negative TgAb in both assays were similar (R2= 0.99; n  = 52). Patients with structural recurrence showed higher Tg values with Tg-LC-MS/MS than with Tg-ECLIA. The undetectable proportion was significantly lower with Tg-LC-MS/MS (31.6%, 6/19) than with Tg-ECLIA (68.4%, 13/19; P  = 0.023). The spike-recovery rate and Tg concentrations determined by the serum mixture text (n  = 29) were significantly reduced to 75.0% (118.3–88.7%) and 81.3% (107.0–87.0%), respectively, with TgAb using Tg-ECLIA (both P  < 0.001) confirming assay interference but not using Tg-LC-MS/MS (91.8–92.3%, P  = 0.77 and 98.4–100.8%, P  = 0.18, respectively).

Conclusions

TgAb had no effect on the Tg-LC-MS/MS assay but yielded 19–25% lower values in Tg-ECLIA. Tg-LC-MS/MS is preferable for monitoring serum Tg levels in TgAb-positive patients, although those with structural recurrence often had disproportionally low Tg values.

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Minoru Kihara Departments of Surgery, Kobe, Japan

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Akira Miyauchi Departments of Surgery, Kobe, Japan

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Hiroshi Yoshida Research, Kuma Hospital, Kobe, Japan

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Osamu Yamada Departments of Surgery, Kobe, Japan

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Hiroo Masuoka Departments of Surgery, Kobe, Japan

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Tomonori Yabuta Departments of Surgery, Kobe, Japan

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Takuya Higashiyama Departments of Surgery, Kobe, Japan

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Mitsuhiro Fukushima Departments of Surgery, Kobe, Japan

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Yasuhiro Ito Departments of Surgery, Kobe, Japan

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Kaoru Kobayashi Departments of Surgery, Kobe, Japan

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Akihiro Miya Departments of Surgery, Kobe, Japan

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A family with germline tandem V804M/Y806C mutations in the RET proto-oncogene was reported. The in vitro study results showing that these mutations were on the same allele and that RET with these mutations had a moderate transforming activity were confirmed by the clinical features of the offspring as a natural experiment. Thus, the tandem double RET mutations are pathogenetic for MEN 2B.

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Naohiro Araki Diagnostic Division, Otsuka Pharmaceutical Co. Ltd., Tokushima, Japan

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Mitsuru Iida Diagnostic Division, Otsuka Pharmaceutical Co. Ltd., Tokushima, Japan

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Nobuyuki Amino Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Shinji Morita Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Akane Ide Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Eijun Nishihara Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Mitsuru Ito Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Jun Saito Department of Medicine, Yokohama Rosai Hospital, Yokohama, Japan

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Tetsuo Nishikawa Department of Medicine, Yokohama Rosai Hospital, Yokohama, Japan

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Kiyonori Katsuragi Diagnostic Division, Otsuka Pharmaceutical Co. Ltd., Tokushima, Japan

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Akira Miyauchi Department of Internal Medicine, Kuma Hospital, Kobe, Japan

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Background: Thyroid-stimulating antibodies (TSAb) are known to be responsible for hyperthyroidism in Graves' disease (GD). The conventional methods to measure TSAb depend on cell-based assays that require cumbersome procedures and a sterilized tissue culture technique. The aim of the present study was to develop a ready-to-use cell-based assay for measuring TSAb activity without requiring sterilized conditions. Methods: We developed a new assay kit using a frozen Chinese hamster ovary cell line expressing the thyroid-stimulating hormone receptor, cyclic adenosine monophosphate (cAMP)-gated calcium channel and aequorin, tentatively named the aequorin TSAb assay. Activated stimulatory G-protein-coupled adenylate cyclase increases intracellular cAMP, which then binds to the cyclic nucleotide-gated calcium channel. Activation of this channel allows Ca<sup>2+</sup> to enter the cell, and the influx of Ca<sup>2+</sup> can be measured with aequorin, which is quantified by a luminometer. Results can be obtained in only 4 h without sterilized conditions. TSAb activities were expressed by international units using the NIBSC 08/204 standard. Results: Positive results of aequorin TSAb were obtained in 197 of 199 (98.9%) of untreated patients with GD. Only 1 of 42 (2.3%) patients with painless thyroiditis had a weakly positive aequorin TSAb. All 45 patients with subacute thyroiditis and 185 normal subjects showed negative aequorin TSAb. As for chronic thyroiditis, all 52 euthyroid patients showed negative aequorin TSAb, but 8 of 50 (16.0%) hypothyroid patients had a positive reaction. However, these positive reactions were not induced by serum thyroid-stimulating hormone (TSH) and were thought to be induced by the stimulating activity of anti-TSH receptor immunoglobulins. Conventional porcine TSAb and Elecsys thyroid-stimulating hormone receptor antibodies were positive in 69.3 and 95.5% of GD, respectively. Conclusion: The aequorin TSAb assay was positive in 98.9% of GD and was more sensitive than the conventional assay. This assay can be conducted in only 4 h without sterilized conditions and is practically useful in general clinical laboratories.

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Akira Miyauchi Departments of Surgery, Kuma Hospital, Kobe, Japan

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Takumi Kudo Departments of Internal Medicine, Kuma Hospital, Kobe, Japan

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Mitsuyoshi Hirokawa Departments of Pathology, Kuma Hospital, Kobe, Japan

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Yasuhiro Ito Departments of Surgery, Kuma Hospital, Kobe, Japan

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Minoru Kihara Departments of Surgery, Kuma Hospital, Kobe, Japan

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Takuya Higashiyama Departments of Surgery, Kuma Hospital, Kobe, Japan

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Tomonori Yabuta Departments of Surgery, Kuma Hospital, Kobe, Japan

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Hiroo Masuoka Departments of Surgery, Kuma Hospital, Kobe, Japan

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Hisakazu Shindo Departments of Surgery, Kuma Hospital, Kobe, Japan

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Kaoru Kobayashi Departments of Surgery, Kuma Hospital, Kobe, Japan

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Akihiro Miya Departments of Surgery, Kuma Hospital, Kobe, Japan

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Background: We previously reported that the Ki-67 labeling index (LI) in primary tumors and the thyroglobulin (Tg)-doubling time (DT) were potent prognostic indicators in patients with papillary thyroid carcinoma (PTC). Objectives: To elucidate the relationship between these two factors. Methods: A total of 390 patients with PTC who underwent total thyroidectomy between 1998 and 2004 and in whom the Tg-DT was calculated were enrolled. We determined the Ki-67 LI in primary tumors and compared these values with the patients' clinicopathological factors, postoperative Tg status, Tg-DT, and prognosis. Tg status was categorized by postoperative serum Tg values: biochemically persistent disease (BPD), equivocal state, and biochemical remission. Results: The Ki-67 LI was ≤5% in 312 patients (80%), 5%-10% in 48 patients (12%), and >10% in 30 patients (8%). Ki-67 LI was significantly associated with BPD (p < 0.0001). The proportion of BPD patients increased with the higher Ki-67 LI category: 24, 67, and 87%, respectively. The Ki-67 LI had a significant inverse correlation with the Tg-DT (Spearman's ρ = −0.5267, p < 0.0001). Of the 378 patients without distant metastasis at surgery, 68 patients had recurrence, and 6 of the 390 patients died of PTC during the follow-up (mean 88 months). On multivariate analyses, the Ki-67 LI remained an independent predictor of disease-free survival and disease-specific survival when Tg-DT and Tg status were excluded from the analyses. Conclusions: Evaluation of the Ki-67 LI in primary tumors may allow the prediction of the postoperative Tg status, Tg-DT and prognosis of patients with PTC.

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Kaoru Kobayashi Kuma Hospital, Kobe, Japan

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Hisashi Ota Kuma Hospital, Kobe, Japan

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Mitsuyoshi Hirokawa Kuma Hospital, Kobe, Japan

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Tomonori Yabuta Kuma Hospital, Kobe, Japan

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Mitsuhiro Fukushima Kuma Hospital, Kobe, Japan

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Hiroo Masuoka Kuma Hospital, Kobe, Japan

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Takuya Higashiyama Kuma Hospital, Kobe, Japan

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Minoru Kihara Kuma Hospital, Kobe, Japan

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Yasuhiro Ito Kuma Hospital, Kobe, Japan

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Akihiro Miya Kuma Hospital, Kobe, Japan

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Akira Miyauchi Kuma Hospital, Kobe, Japan

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Background: It is generally considered impossible to differentiate follicular carcinomas from follicular adenomas by means of ultrasonography or cytology before surgery. Therefore, follicular carcinoma is histopathologically diagnosed by verifying capsular and/or vascular invasion after surgery. However, ultrasonography may play an important role in diagnosing follicular carcinoma preoperatively in a small number of cases. Case Description: Four cases of follicular carcinoma or follicular neoplasm that transformed from a benign thyroid tumor and demonstrated a “nodule in nodule” appearance on ultrasonography are presented in this report. Characteristic ultrasound features of such patients are: (1) a “nodule in nodule” appearance, (2) a well-defined boundary line between the nodules, and (3) separate distribution of blood signals within each nodule. Conclusion: A small number of patients with follicular carcinomas or follicular neoplasms may present with a “nodule in nodule” appearance on ultrasonography. It was suggested a long time ago that follicular carcinomas may develop from benign thyroid tumors. The fact that follicular carcinomas appear within benign tumors may be evidence of thyroid tumorigenesis.

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