International Journal of Endocrinology and Metabolism

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Insulin Resistance Associated With Differentiated Thyroid Carcinoma: Penalized Conditional Logistic Regression Analysis of a Matched Case-Control Study Data

Zahra Heidari 1 , Mahdi Abdani 1 and Mohammad Ali Mansournia 2 , *
Authors Information
1 MD, Department of Endocrinology and Metabolism, Zahedan University of Medical Sciences, Zahedan, IR Iran
2 MD, MPH, PhD, Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, IR Iran
Article information
  • International Journal of Endocrinology and Metabolism: January 2018, 16 (1); e14545
  • Published Online: October 25, 2017
  • Article Type: Research Article
  • Received: June 26, 2017
  • Revised: September 7, 2017
  • Accepted: October 4, 2017
  • DOI: 10.5812/ijem.14545

To Cite: Heidari Z, Abdani M, Mansournia M A. Insulin Resistance Associated With Differentiated Thyroid Carcinoma: Penalized Conditional Logistic Regression Analysis of a Matched Case-Control Study Data, Int J Endocrinol Metab. 2018 ; 16(1):e14545. doi: 10.5812/ijem.14545.

Copyright © 2017, International Journal of Endocrinology and Metabolism. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Methods
3. Results
4. Discussion
  • 1. Davies L, Morris LG, Haymart M, Chen AY, Goldenberg D, Morris J, et al. American Association of Clinical Endocrinologists and American College of Endocrinology Disease State Clinical Review: The Increasing Incidence of Thyroid Cancer. Endocr Pract. 2015;21(6):686-96. doi: 10.4158/EP14466.DSCR. [PubMed: 26135963].
  • 2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90. doi: 10.3322/caac.20107. [PubMed: 21296855].
  • 3. Amphlett B, Lawson Z, Abdulrahman GJ, White C, Bailey R, Premawardhana LD, et al. Recent trends in the incidence, geographical distribution, and survival from thyroid cancer in Wales, 1985-2010. Thyroid. 2013;23(11):1470-8. doi: 10.1089/thy.2012.0573. [PubMed: 23488941].
  • 4. Colonna M, Uhry Z, Guizard AV, Delafosse P, Schvartz C, Belot A, et al. Recent trends in incidence, geographical distribution, and survival of papillary thyroid cancer in France. Cancer Epidemiol. 2015;39(4):511-8. doi: 10.1016/j.canep.2015.04.015. [PubMed: 26003877].
  • 5. Jung KW, Won YJ, Oh CM, Kong HJ, Lee DH, Lee KH, et al. Cancer Statistics in Korea: Incidence, Mortality, Survival, and Prevalence in 2014. Cancer Res Treat. 2017;49(2):292-305. doi: 10.4143/crt.2017.118. [PubMed: 28279062].
  • 6. Kent WD, Hall SF, Isotalo PA, Houlden RL, George RL, Groome PA. Increased incidence of differentiated thyroid carcinoma and detection of subclinical disease. CMAJ. 2007;177(11):1357-61. doi: 10.1503/cmaj.061730. [PubMed: 18025426].
  • 7. 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):784-91. doi: 10.1158/1055-9965.EPI-08-0960. [PubMed: 19240234].
  • 8. Dom G, Tarabichi M, Unger K, Thomas G, Oczko-Wojciechowska M, Bogdanova T, et al. A gene expression signature distinguishes normal tissues of sporadic and radiation-induced papillary thyroid carcinomas. Br J Cancer. 2012;107(6):994-1000. doi: 10.1038/bjc.2012.302. [PubMed: 22828612].
  • 9. 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):242-52. doi: 10.1093/aje/kwp354. [PubMed: 19951937].
  • 10. Borena W, Stocks T, Jonsson H, Strohmaier S, Nagel G, Bjorge T, et al. Serum triglycerides and cancer risk in the metabolic syndrome and cancer (Me-Can) collaborative study. Cancer Causes Control. 2011;22(2):291-9. doi: 10.1007/s10552-010-9697-0. [PubMed: 21140204].
  • 11. Zhao ZG, Guo XG, Ba CX, Wang W, Yang YY, Wang J, et al. Overweight, obesity and thyroid cancer risk: a meta-analysis of cohort studies. J Int Med Res. 2012;40(6):2041-50. doi: 10.1177/030006051204000601. [PubMed: 23321160].
  • 12. Rezzonico JN, Rezzonico M, Pusiol E, Pitoia F, Niepomniszcze H. Increased prevalence of insulin resistance in patients with differentiated thyroid carcinoma. Metab Syndr Relat Disord. 2009;7(4):375-80. doi: 10.1089/met.2008.0062. [PubMed: 19320560].
  • 13. Biondi B, Arpaia D, Montuori P, Ciancia G, Ippolito S, Pettinato G, et al. Under the shadow of vesuvius: a risk for thyroid cancer?. Thyroid. 2012;22(12):1296-7. doi: 10.1089/thy.2012.0002. [PubMed: 23083444].
  • 14. Pellegriti G, De Vathaire F, Scollo C, Attard M, Giordano C, Arena S, et al. Papillary thyroid cancer incidence in the volcanic area of Sicily. J Natl Cancer Inst. 2009;101(22):1575-83. doi: 10.1093/jnci/djp354. [PubMed: 19893009].
  • 15. Jung SK, Kim K, Tae K, Kong G, Kim MK. The effect of raw vegetable and fruit intake on thyroid cancer risk among women: a case-control study in South Korea. Br J Nutr. 2013;109(1):118-28. doi: 10.1017/S0007114512000591. [PubMed: 22455656].
  • 16. Clero E, Doyon F, Chungue V, Rachedi F, Boissin JL, Sebbag J, et al. Dietary patterns, goitrogenic food, and thyroid cancer: a case-control study in French Polynesia. Nutr Cancer. 2012;64(7):929-36. doi: 10.1080/01635581.2012.713538. [PubMed: 23061901].
  • 17. Bessesen DH. Update on obesity. J Clin Endocrinol Metab. 2008;93(6):2027-34. doi: 10.1210/jc.2008-0520. [PubMed: 18539769].
  • 18. Vella V, Sciacca L, Pandini G, Mineo R, Squatrito S, Vigneri R, et al. The IGF system in thyroid cancer: new concepts. Mol Pathol. 2001;54(3):121-4. [PubMed: 11376121].
  • 19. Balkan F, Onal ED, Usluogullari A, Tuzun D, Ozdemir D, Inancli SS, et al. "Is there any association between insulin resistance and thyroid cancer? : A case control study". Endocrine. 2014;45(1):55-60. doi: 10.1007/s12020-013-9942-x. [PubMed: 23564559].
  • 20. Spencer CA, Takeuchi M, Kazarosyan M. Current status and performance goals for serum thyrotropin (TSH) assays. Clin Chem. 1996;42(1):140-5. [PubMed: 8565217].
  • 21. Kratzsch J, Fiedler GM, Leichtle A, Brugel M, Buchbinder S, Otto L, et al. New reference intervals for thyrotropin and thyroid hormones based on National Academy of Clinical Biochemistry criteria and regular ultrasonography of the thyroid. Clin Chem. 2005;51(8):1480-6. doi: 10.1373/clinchem.2004.047399. [PubMed: 15961550].
  • 22. Delshad H, Mehran L, Azizi F. Appropriate iodine nutrition in Iran: 20 years of success. Acta Med Iran. 2010;48(6):361-6. [PubMed: 21287473].
  • 23. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412-9. [PubMed: 3899825].
  • 24. Ascaso JF, Pardo S, Real JT, Lorente RI, Priego A, Carmena R. Diagnosing insulin resistance by simple quantitative methods in subjects with normal glucose metabolism. Diabetes Care. 2003;26(12):3320-5. [PubMed: 14633821].
  • 25. Yokoyama H, Emoto M, Fujiwara S, Motoyama K, Morioka T, Komatsu M, et al. Quantitative insulin sensitivity check index and the reciprocal index of homeostasis model assessment in normal range weight and moderately obese type 2 diabetic patients. Diabetes Care. 2003;26(8):2426-32. [PubMed: 12882874].
  • 26. Mansournia MA, Altman DG. Invited commentary: methodological issues in the design and analysis of randomised trials. Br J Sports Med. 2017. doi: 10.1136/bjsports-2017-098245. [PubMed: 28756393].
  • 27. Greenland S, Mansournia MA. Limitations of individual causal models, causal graphs, and ignorability assumptions, as illustrated by random confounding and design unfaithfulness. Eur J Epidemiol. 2015;30(10):1101-10. doi: 10.1007/s10654-015-9995-7. [PubMed: 25687168].
  • 28. Mansournia MA, Hernan MA, Greenland S. Matched designs and causal diagrams. Int J Epidemiol. 2013;42(3):860-9. doi: 10.1093/ije/dyt083. [PubMed: 23918854].
  • 29. Mansournia MA, Jewell NP, Greenland S. Case-control matching: effects, misconceptions, and recommendations. Eur J Epidemiol. 2017:[Epub ahead of print]. doi: 10.1007/s10654-017-0325-0.
  • 30. Greenland S, Mansournia MA, Altman DG. Sparse data bias: a problem hiding in plain sight. BMJ. 2016;352. i1981. doi: 10.1136/bmj.i1981. [PubMed: 27121591].
  • 31. Mansournia MA, Geroldinger A, Greenland S, Heinze G. Separation in Logistic Regression - Causes, Consequences, and Control. Am J Epidemiol. 2017. doi: 10.1093/aje/kwx299. [PubMed: 29020135].
  • 32. Rezzonico J, Rezzonico M, Pusiol E, Pitoia F, Niepomniszcze H. Introducing the thyroid gland as another victim of the insulin resistance syndrome. Thyroid. 2008;18(4):461-4. doi: 10.1089/thy.2007.0223. [PubMed: 18346005].
  • 33. Junik R, Kozinski M, Debska-Kozinska K. Thyroid ultrasound in diabetic patients without overt thyroid disease. Acta Radiol. 2006;47(7):687-91. doi: 10.1080/02841850600806308. [PubMed: 16950706].
  • 34. Rezzonico J, Rezzonico M, Pusiol E, Pitoia F, Niepomniszcze H. Metformin treatment for small benign thyroid nodules in patients with insulin resistance. Metab Syndr Relat Disord. 2011;9(1):69-75. doi: 10.1089/met.2010.0026. [PubMed: 21128816].
  • 35. Rezzonico J, Rezzonico M, Pusiol E, Pitoia F, Niepomniszcze H. High prevalence of thyroid nodules in patients with achrocordons (skin tags). Possible role of insulin-resistance. Medicina (B Aires). 2009;69(3):302-4. [PubMed: 19622476].
  • 36. Ayturk S, Gursoy A, Kut A, Anil C, Nar A, Tutuncu NB. Metabolic syndrome and its components are associated with increased thyroid volume and nodule prevalence in a mild-to-moderate iodine-deficient area. Eur J Endocrinol. 2009;161(4):599-605. doi: 10.1530/EJE-09-0410. [PubMed: 19633072].
  • 37. Heidari Z, Mashhadi MA, Nosratzehi S. Insulin Resistance in Patients with Benign Thyroid Nodules. Arch Iran Med. 2015;18(9):572-6. [PubMed: 26317597].
  • 38. Haggar FA, Preen DB, Pereira G, Holman CD, Einarsdottir K. Cancer incidence and mortality trends in Australian adolescents and young adults, 1982-2007. BMC Cancer. 2012;12:151. doi: 10.1186/1471-2407-12-151. [PubMed: 22520938].
  • 39. Ellison LF, Wilkins K. Canadian trends in cancer prevalence. Health Rep. 2012;23(1):7-16. [PubMed: 22590801].
  • 40. Dal Maso L, Lise M, Zambon P, Falcini F, Crocetti E, Serraino D, et al. Incidence of thyroid cancer in Italy, 1991-2005: time trends and age-period-cohort effects. Ann Oncol. 2011;22(4):957-63. doi: 10.1093/annonc/mdq467. [PubMed: 20952599].
  • 41. Li C, Ford ES, McGuire LC, Mokdad AH, Little RR, Reaven GM. Trends in hyperinsulinemia among nondiabetic adults in the U.S. Diabetes Care. 2006;29(11):2396-402. doi: 10.2337/dc06-0289. [PubMed: 17065674].
  • 42. Gursoy A. Rising thyroid cancer incidence in the world might be related to insulin resistance. Med Hypotheses. 2010;74(1):35-6. doi: 10.1016/j.mehy.2009.08.021. [PubMed: 19720470].
  • 43. 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):631-56. doi: 10.1210/edrv.22.5.0444. [PubMed: 11588145].
  • 44. Riedemann J, Macaulay VM. IGF1R signalling and its inhibition. Endocr Relat Cancer. 2006;13 Suppl 1:S33-43. doi: 10.1677/erc.1.01280. [PubMed: 17259557].
  • 45. Malaguarnera R, Frasca F, Garozzo A, Giani F, Pandini G, Vella V, et al. Insulin receptor isoforms and insulin-like growth factor receptor in human follicular cell precursors from papillary thyroid cancer and normal thyroid. J Clin Endocrinol Metab. 2011;96(3):766-74. doi: 10.1210/jc.2010-1255. [PubMed: 21123448].
  • 46. Namba H, Nakashima M, Hayashi T, Hayashida N, Maeda S, Rogounovitch TI, et al. Clinical implication of hot spot BRAF mutation, V599E, in papillary thyroid cancers. J Clin Endocrinol Metab. 2003;88(9):4393-7. doi: 10.1210/jc.2003-030305. [PubMed: 12970315].
  • 47. Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA. High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res. 2003;63(7):1454-7. [PubMed: 12670889].
  • 48. Rapoport B, Chazenbalk GD, Jaume JC, McLachlan SM. The thyrotropin (TSH) receptor: interaction with TSH and autoantibodies. Endocr Rev. 1998;19(6):673-716. doi: 10.1210/edrv.19.6.0352. [PubMed: 9861544].
  • 49. Freedman DM, Looker AC, Abnet CC, Linet MS, Graubard BI. Serum 25-hydroxyvitamin D and cancer mortality in the NHANES III study (1988-2006). Cancer Res. 2010;70(21):8587-97. doi: 10.1158/0008-5472.CAN-10-1420. [PubMed: 20847342].
  • 50. Macejova D, Ondkova S, Brtko J. Vitamin D3 affects expression of thyroid hormone receptor alpha and deiodinase activity in liver of MNU-treated Sprague-Dawley rats. Gen Physiol Biophys. 2009;28(4):363-70. [PubMed: 20097959].
  • 51. Sfanos KS, De Marzo AM. Prostate cancer and inflammation: the evidence. Histopathology. 2012;60(1):199-215. doi: 10.1111/j.1365-2559.2011.04033.x. [PubMed: 22212087].
  • 52. Greenland S, Mansournia MA. Penalization, bias reduction, and default priors in logistic and related categorical and survival regressions. Stat Med. 2015;34(23):3133-43. doi: 10.1002/sim.6537. [PubMed: 26011599].
  • 53. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004;27(6):1487-95. [PubMed: 15161807].
  • 54. Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care. 1998;21(12):2191-2. [PubMed: 9839117].

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