Int J Thyroidol.  2019 May;12(1):44-53. 10.11106/ijt.2019.12.1.44.

High Body Mass Index and Thyroid Stimulating Hormone Levels Do Not Affect Thyroid Nodule Selection for Fine-Needle Aspiration Biopsy after Ultrasound Evaluation

• Kim HG
• Lee HS
• Kim EK
• Nam CM
• Moon HJ
• Jung HK
• Kwak JY

• KMID: 2449065
• DOI: http://doi.org/10.11106/ijt.2019.12.1.44

Abstract

BACKGROUND AND OBJECTIVES
This study was to evaluate whether high body mass index (BMI) or thyroid stimulating hormone (TSH) level would affect selecting thyroid nodule for fine-needle aspiration biopsy (FNA) after ultrasound (US) evaluation.
MATERIALS AND METHODS
A total of 3155 thyroid nodules (2159 benign and 996 malignant nodules) were included. Four grades of BMI and three levels of TSH were applied for grouping. US features of the thyroid nodules were divided into "˜probably benign' and "˜suspicious for malignancy' categories. Patients were grouped according to gender and univariate and multivariate logistic regression analysis were used to find the association between variables and malignancy.
RESULTS
TSH levels were significantly higher in the malignant group (p<0.001). The grades of BMI did not show difference between the malignant and benign groups (females, p=0.074 and males, p=0.157). Younger age and "˜suspicious for malignancy' US category were independent risk factors for malignancy in both genders. In females, a high TSH level (odds ratio=1.010, p<0.001) had significant association with malignancy. Except for younger age (odds ratio=0.998, p<0.001), no variable in nodules with "˜probably benign' US category was significantly associated with malignancy.
CONCLUSION
High TSH levels were more frequent in thyroid malignancy group, but neither high BMI nor high TSH level give additional information for FNA selection after US.

Keyword

Thyroid cancer; Ultrasound; Obesity; Thyroid stimulating hormone; Fine-needle aspiration biopsy

MeSH Terms

Biopsy, Fine-Needle*
Body Mass Index*
Female
Humans
Logistic Models
Male
Obesity
Risk Factors
Thyroid Gland*
Thyroid Neoplasms
Thyroid Nodule*
Thyrotropin*
Ultrasonography*
Thyrotropin

Reference

1. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA. 2006; 295(18):2164–2167.

2. Jung KW, Park S, Kong HJ, Won YJ, Lee JY, Park EC, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2008. Cancer Res Treat. 2011; 43(1):1–11.

3. Enewold L, Zhu K, Ron E, Marrogi AJ, Stojadinovic A, Peoples GE, et al. Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980-2005. Cancer Epidemiol Biomarkers Prev. 2009; 18(3):784–791.

4. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer. Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009; 19(11):1167–1214.

5. Meinhold CL, Ron E, Schonfeld SJ, Alexander BH, Freedman DM, Linet MS, et al. Nonradiation risk factors for thyroid cancer in the US Radiologic Technologists Study. Am J Epidemiol. 2010; 171(2):242–252.

6. Ogden CL, Yanovski SZ, Carroll MD, Flegal KM. The epidemiology of obesity. Gastroenterology. 2007; 132(6):2087–2102.

7. Kitahara CM, Platz EA, Freeman LE, Hsing AW, Linet MS, Park Y, et al. Obesity and thyroid cancer risk among U.S. men and women: A pooled analysis of five prospective studies. Cancer Epidemiol Biomarkers Prev. 2011; 20(3):464–472.

8. Han JM, Kim TY, Jeon MJ, Yim JH, Kim WG, Song DE, et al. Obesity is a risk factor for thyroid cancer in a large, ultrasonographically screened population. Eur J Endocrinol. 2013; 168(6):879–886.

9. Kim HK, Yoon JH, Kim SJ, Cho JS, Kweon SS, Kang HC. Higher TSH level is a risk factor for differentiated thyroid cancer. Clin Endocrinol (Oxf). 2013; 78(3):472–477.

10. Haymart MR, Repplinger DJ, Leverson GE, Elson DF, Sippel RS, Jaume JC, et al. Higher serum thyroid stimulating hormone level in thyroid nodule patients is associated with greater risks of differentiated thyroid cancer and advanced tumor stage. J Clin Endocrinol Metab. 2008; 93(3):809–814.

11. Boelaert K, Horacek J, Holder RL, Watkinson JC, Sheppard MC, Franklyn JA. Serum thyrotropin concentration as a novel predictor of malignancy in thyroid nodules investigated by fine-needle aspiration. J Clin Endocrinol Metab. 2006; 91(11):4295–4301.

12. Diez JJ, Iglesias P. Relationship between thyrotropin and body mass index in euthyroid subjects. Exp Clin Endocrinol Diabetes. 2011; 119(3):144–150.

13. Fox CS, Pencina MJ, D'Agostino RB, Murabito JM, Seely EW, Pearce EN, et al. Relations of thyroid function to body weight: cross-sectional and longitudinal observations in a community-based sample. Arch Intern Med. 2008; 168(6):587–592.

14. Rotondi M, Leporati P, La Manna A, Pirali B, Mondello T, Fonte R, et al. Raised serum TSH levels in patients with morbid obesity: is it enough to diagnose subclinical hypothyroidism? Eur J Endocrinol. 2009; 160(3):403–408.

15. Kwak JY, Kim EK, Kim HJ, Kim MJ, Son EJ, Moon HJ. How to combine ultrasound and cytological information in decision making about thyroid nodules. Eur Radiol. 2009; 19(8):1923–1931.

16. Kwak JY, Koo H, Youk JH, Kim MJ, Moon HJ, Son EJ, et al. Value of US correlation of a thyroid nodule with initially benign cytologic results. Radiology. 2010; 254(1):292–300.

17. Moon HJ, Kwak JY, Kim EK, Choi JR, Hong SW, Kim MJ, et al. The role of BRAFV600E mutation and ultrasonography for the surgical management of a thyroid nodule suspicious for papillary thyroid carcinoma on cytology. Ann Surg Oncol. 2009; 16(11):3125–3131.

18. Yoon JH, Moon HJ, Kim EK, Kwak JY. Inadequate cytology in thyroid nodules: should we repeat aspiration or follow-up? Ann Surg Oncol. 2011; 18(5):1282–1289.

19. World Health Organization Technical Report Series 894. Obesity: Preventing and managing the global epidemic. Geneva, Switzerland: World Health Organization;2000.

20. Kim EK, Park CS, Chung WY, Oh KK, Kim DI, Lee JT, et al. New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am J Roentgenol. 2002; 178(3):687–691.

21. Iacobellis G, Ribaudo MC, Zappaterreno A, Iannucci CV, Leonetti F. Relationship of thyroid function with body mass index, leptin, insulin sensitivity and adiponectin in euthyroid obese women. Clin Endocrinol (Oxf). 2005; 62(4):487–491.

22. Kim B. Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate. Thyroid. 2008; 18(2):141–144.

23. Reinehr T. Obesity and thyroid function. Mol Cell Endocrinol. 2010; 316(2):165–171.

24. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996; 334(5):292–295.

25. Marzullo P, Minocci A, Tagliaferri MA, Guzzaloni G, Di Blasio A, De Medici C, et al. Investigations of thyroid hormones and antibodies in obesity: Leptin levels are associated with thyroid autoimmunity independent of bioanthropometric, hormonal, and weight-related determinants. J Clin Endocrinol Metab. 2010; 95(8):3965–3972.

26. Pazaitou-Panayiotou K, Polyzos SA, Mantzoros CS. Obesity and thyroid cancer: Epidemiologic associations and underlying mechanisms. Obes Rev. 2013; 14(12):1006–1022.

27. Kimura T, Van Keymeulen A, Golstein J, Fusco A, Dumont JE, Roger PP. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr Rev. 2001; 22(5):631–656.

28. McLeod DS, Watters KF, Carpenter AD, Ladenson PW, Cooper DS, Ding EL. Thyrotropin and thyroid cancer diagnosis: a systematic review and dose-response meta-analysis. J Clin Endocrinol Metab. 2012; 97(8):2682–2692.

29. Mazzaferri EL. Thyroid cancer and Graves' disease: the controversy ten years later. Endocr Pract. 2000; 6(2):221–225.

30. Park J, Kim WG, Zhao L, Enomoto K, Willingham M, Cheng SY. Metformin blocks progression of obesity-activated thyroid cancer in a mouse model. Oncotarget. 2016; 7(23):34832–34844.

31. Shi Y, Zou M, Farid NR. Expression of thyrotrophin receptor gene in thyroid carcinoma is associated with a good prognosis. Clin Endocrinol (Oxf). 1993; 39(3):269–274.

32. Fiore E, Rago T, Provenzale MA, Scutari M, Ugolini C, Basolo F, et al. Lower levels of TSH are associated with a lower risk of papillary thyroid cancer in patients with thyroid nodular disease: thyroid autonomy may play a protective role. Endocr Relat Cancer. 2009; 16(4):1251–1260.

33. Balakrishnan VS. Low BMI linked to worse colorectal cancer outcomes. Lancet Oncol. 2015; 16(16):e593.

34. Nakagawa T, Toyazaki T, Chiba N, Ueda Y, Gotoh M. Prognostic value of body mass index and change in body weight in postoperative outcomes of lung cancer surgery. Interact Cardiovasc Thorac Surg. 2016; 23(4):560–566.

35. Keinan-Boker L, Levine H, Derazne E, Molina-Hazan V, Kark JD. Measured adolescent body mass index and adult breast cancer in a cohort of 951,480 women. Breast Cancer Res Treat. 2016; 158(1):157–167.

36. Magister MJ, Chaikhoutdinov I, Schaefer E, Williams N, Saunders B, Goldenberg D. Association of thyroid nodule size and Bethesda class with rate of malignant disease. JAMA Otolaryngol Head Neck Surg. 2015; 141(12):1089–1095.

37. Cavallo A, Johnson DN, White MG, Siddiqui S, Antic T, Mathew M, et al. Thyroid nodule size at ultrasound as a predictor of malignancy and final pathologic size. Thyroid. 2017; 27(5):641–650.

38. Kamran SC, Marqusee E, Kim MI, Frates MC, Ritner J, Peters H, et al. Thyroid nodule size and prediction of cancer. J Clin Endocrinol Metab. 2013; 98(2):564–570.

39. Hong MJ, Na DG, Baek JH, Sung JY, Kim JH. Impact of nodule size on malignancy risk differs according to the ultrasonography pattern of thyroid nodules. Korean J Radiol. 2018; 19(3):534–541.

40. Lee MJ, Hong SW, Chung WY, Kwak JY, Kim MJ, Kim EK. Cytological results of ultrasound-guided fine-needle aspiration cytology for thyroid nodules: emphasis on correlation with sonographic findings. Yonsei Med J. 2011; 52(5):838–844.

41. Mehany MT, El Kolaly MT, Annyoub SM, Hassan SEM. Immunoradiometric assay for the in-vitro determination of thyroid stimulating hormone in human serum and plasma using solid phase anti-TSH cellulose particles. J Radioanal Nucl Chem. 2005; 265(1):61–71.