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Evaluation of the Thyroid Characteristics of Patients with Growth Hormone-Secreting Adenomas

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Evaluation of the Thyroid Characteristics of Patients with Growth Hormone-Secreting Adenomas Xu et al. BMC Endocrine Disorders (2019) 19:94 https://doi.org/10.1186/s12902-019-0424-x RESEARCHARTICLE Open Access Evaluation of the thyroid characteristics of patients with growth hormone-secreting adenomas Dianshuang Xu1†, Bolin Wu1†, Xiaoju Li2, Yunjiu Cheng3, Dubo Chen4, Yuefeng Fang5, Qiu Du6, Zhiyong Chen1* and Xiaodong Wang1* Abstract Background: Acromegaly is highly associated with thyroid disorders. However, the clinical characteristics of thyroid nodules in individuals with acromegaly who present with thyroid diseases have not been completely elucidated. Methods: Overall, 134 consecutive participants with growth hormone (GH)-secreting adenoma (n = 67) and non- functioning (NF) pituitary adenoma (n = 67) were recruited from the outpatient and inpatient patient department of The First Affiliated Hospital, Jinan University from August 2015 to August 2017. Thyroid ultrasonography was performed using an ultrasound system. The cytopathological results of fine-needle aspiration biopsy were analyzed by a pathologist according to the Bethesda system. Twenty-one patients with GH-secreting adenoma and thyroid disease underwent transsphenoidal pituitary adenoma resection and were followed up for 1 year. Results: The prevalence of thyroid disease increased in the GH-secreting adenoma group compared with that in the NF pituitary adenoma group. The number of hypoechoic, isoechogenic, heterogeneous, and vascular thyroid nodules increased in patients with GH-secreting adenoma plus thyroid disease compared with that in patients with NF pituitary adenoma plus thyroid disease. Finally, we found significant decreases in the morphology of solid nodules and significant increases in the morphology of cystic nodules after surgery compared with those before surgery in the cured group. Moreover, the numbers of heterogeneous and vascular thyroid nodules decreased significantly after surgery compared with those before surgery in the cured group. However, the characteristics of the thyroid nodules did not change after surgery compared with thosebeforesurgeryinthenon-curedgroup. Conclusions: The numbers of hypoechoic, isoechoic, heterogeneous, and vascular thyroid nodules increased in patients with GH-secreting adenomas. In these patients, surgery resulted in significant changes from solid to cystic nodules and also reduced the numbers of heterogeneous and vascular thyroid nodules. Keywords: Thyroid disease, Growth hormone secretingadenomas,Thyroidnodules,Ultrasound Background [3–5]. Golkowski et al. reported goiter in 85 (75.2%) Pituitary adenoma is a chronic endocrine disease that is of 113 patients with acromegaly [6]. In addition, characterized by the excessive secretion of growth hormone Roqozinski et al. observed nodular thyroid disorders (GH) and insulin-like growth factor I (IGF-I), which results in 23 (67%) of 34 patients with acromegaly [5]. Moreover, in various physiological abnormities [1, 2]. Increasing Gasperi et al. reported that 202 (78.3%) of 258 patients with evidence has shown that many individuals with acro- acromegaly and 28 (10.8%) of 258 patients with non-func- megaly also present with various thyroid abnormities tioning prolactin-secreting pituitary adenomas were diag- nosed with thyroid disorders [7]. Furthermore, the risk of * Correspondence: [email protected]; [email protected] † thyroid cancer is high in patients with acromegaly [8, 9]. Dianshuang Xu and Bolin Wu contributed equally to this work. The results of these studies indicate that the thyroid is the 1Department of Neurosurgery, The First Affiliated Hospital, Jinan University, No. 613 Huangpu Avenue West, Tianhe District, Guangzhou 510632, most frequently affected organ in patients with acromegaly; Guangdong Province 510630, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Xu et al. BMC Endocrine Disorders (2019) 19:94 Page 2 of 9 hence, the correlation between acromegaly and thyroid approval was obtained by the ethics committee of The disorders has become a topic of interest. First Affiliated Hospital, Jinan University. The development of thyroid nodules is caused by the abnormal proliferation of thyroid cells. The characteris- Endocrine examination and MRI tics of thyroid nodules, including the number of nodules Venous blood was collected from all participants after (single or multiple), morphology (solid, mixed, or cystic), they had fasted for 8–10 h. Levels of GH, IGF-1, and position (right, left, or gorge), echogenicity (hypoechoic, other pituitary endocrine hormones were measured isoechogenic, hyperechoic, or none), echotexture (homoge- using a chemiluminescent immunoassay system. Con- neous or heterogeneous), margin (regular or irregular), cal- ventional and enhanced MRI scans of the pituitary gland cification (none, micro-calcification, or macro-calcification), were performed on all patients. The steps of the proced- and blood vessels (none, rare, or abundant), can be used as ure were as described in our previous studies [11]. a basis for diagnosis [10]. However, the clinical characteris- tics of thyroid nodules in patients with acromegaly who Ultrasonography were diagnosed with thyroid disease remain unclear. Thyroid ultrasonography was performed by a practi- This retrospective study analyzed the incidence of tioner using an iU22 xMatrix-DS Ultrasound system thyroid disease and the characteristics of thyroid nod- (PHILIPS, 795112) with a 3–12-MHz linear transducer. ules in patients with active growth hormone (GH)-se- The thyroid volume was calculated using the volume creting and non-functioning (NF) pituitary adenomas. formula for an ellipsoid model (π/6 × width × length × We also analyzed the characteristics of thyroid nodules thickness). The sum of the volume of each thyroid lobe in patients with GH-secreting adenoma after surgery. and isthmus was defined as the total thyroid volume [7]. This study was conducted to better understand the cor- Goiter was defined as a thyroid volume greater than relation between acromegaly and the characteristics of 12.6 cm3 in women and 17.1 cm3 in men. After deter- thyroid nodules. mining the thyroid volume, the patients were classified into the normal, diffuse goiter, and nodular goiter Methods groups according to the thyroid morphology. Participants All 134 consecutive participants with GH-secreting (n = Fine-needle aspiration biopsy (FNAB) 67) and NF pituitary (n = 67) adenomas were recruited FNAB was performed by a practitioner on patients with from the outpatient and inpatient department of The nodule volume exceeding 1 cm3 or a node with two or First Affiliated Hospital, Jinan University between August more of diverse signals: 1) hypoechoic nodules, 2) hazy 2015 and August 2017. After obtaining clinical parame- nodular border, 3) uneven internal echo, 4) abundant ters, such as age, sex, weight, basal metabolic rate, body blood flow in the middle of the nodule, 5) multifocal mass index, heart rate, and blood pressure, the patients strong echo, and 6) tophaceous calcification. The cyto- were assessed for the signs and symptoms of thyroid dis- pathological results were analyzed by the same patholo- eases. After measuring hormone levels and conducting gist according to the Bethesda system [12]. ultrasonography, the patients were divided into two groups: those with pituitary adenoma who presented with Treatment and follow-up asaddleareaoncomputedtomography(CT)scanor Forty-seven patients with GH-secreting adenoma and magnetic resonance imaging (MRI), low serum IGF-1 thyroid disease underwent relevant examinations and levels, or pituitrin or prolactin levels < 100 ng/mL (NF pi- transsphenoidal pituitary adenoma resection, while three tuitary adenoma group) and those with one of following patients with thyroid cancer underwent thyroidectomy. symptoms: presence of a pituitary adenoma as character- All three patients with cancer and 23 other patients were ized by a saddle area on CT scan or MRI, high serum lost to follow-up and were excluded from the study. IGF-1 levels, GH levels > 2.5 ng/mL, and low GH suppres- After the 1-year follow-up, clinically relevant data from sion (< 2 ng/mL) after the oral administration of 75 g of the remaining patients (n = 21) were collected. glucose (GH-secreting adenoma group). The exclusion criteria were as follows: 1) pregnant and lactating women, Statistical analysis 2) those with psychiatric disorders, 3) those with pituitary Statistical analyses were performed using IBM SPSS Sta- disease diagnosed before acromegaly, 4) those who under- tistics for Windows, version 19.0, and the results were went thyroidectomy, 5) those who smoked or consumed expressed as medians (minimum-maximum). Pairwise alcohol, 6) those aged older than 70 years or younger than comparisons were conducted using Wilcoxon rank-sum 20 years, and 7) those with other aggressive types of can- tests. f: Fisher’ exact test: 1) chi-square tests for n <40 cer. Prior
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