Skip to main content

Advertisement

SpringerLink
Log in

Association of obesity and diabetes with thyroid nodules

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Aim

There are conflicting data concerning the possibility that obesity and diabetes raise the risk of thyroid nodules. The incidence of thyroid nodules is increasing, as is that of obesity and diabetes; therefore, understanding whether these metabolic and nutritional disorders influence nodular thyroid disease is important for organizing prevention strategies. This study investigated the association between thyroid nodules, obesity, diabetes, and dietary habits.

Materials and methods

A cohort of randomly selected adults (455 males, 746 females; age: 18–90 years) living in Palermo (Italy), a mild iodine deficiency area, was cross-sectionally investigated. Participants underwent high-resolution ultrasonographic evaluation of the thyroid, and answered a food frequency questionnaire. Laboratory blood measurements were obtained in 587 participants.

Results and discussion

Thyroid nodules were detected in 475 (39.5%) participants. The number of thyroid nodules was correlated with age (r = 0.19; P < 0.001), gender (r = 0.08; P = 0.005), and body mass index (r = 0.07; P = 0.02). No significant correlation was observed between the number of nodules and glycated hemoglobin, serum insulin concentrations, and homeostasis model assessment of insulin resistance. Age-adjusted and gender-adjusted prevalence of both overweight/obesity and type 2 diabetes of each group of participants divided according to the number of nodules significantly increased with the number of nodules (P < 0.05 in both cases). The group of participants with nodules exhibited a significantly lower age-adjusted and gender-adjusted habitual intake of milk (P = 0.02). Multivariate regression analysis showed that age, gender, body mass index, diabetes, and habitual consumption of milk were independently correlated with presence of thyroid nodules.

Conclusion

This study seems to indicate that an association exists between obesity, diabetes, and thyroid nodules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. E.L. Mazzaferri, Management of a solitary thyroid nodule. N. Engl. J. Med. 328, 553–559 (1993). doi:10.1056/NEJM199302253280807

    Article  CAS  PubMed  Google Scholar 

  2. B. D’Avanzo, C. La Vecchia, S. Franceschi, E. Negri, R. Talamini, History of thyroid diseases and subsequent thyroid cancer risk. Cancer Epidemiol. Biomark. Prev. 4, 193–199 (1995)

    Google Scholar 

  3. N. Arora, T. Scognamiglio, B. Zhu, T.J. Fahey, 3rd: do benign thyroid nodules have malignant potential? An evidence-based review. World J. Surg. 32, 1237–1246 (2008). doi:10.1007/s00268-008-9484-1

    Article  PubMed  Google Scholar 

  4. L. Davies, H.G. Welch, Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295, 2164–2167 (2006). doi:10.1001/jama.295.18.2164

    Article  CAS  PubMed  Google Scholar 

  5. M. Colonna, P. Grosclaude, L. Remontet, C. Schvartz, J. Mace-Lesech, M. Velten et al. Incidence of thyroid cancer in adults recorded by French cancer registries (1978–1997). Eur. J. Cancer 38, 1762–1768 (2002)

    Article  CAS  PubMed  Google Scholar 

  6. L. Hegedüs, S.J. Bonnema, F.N. Bennedbæk, Management of simple nodular goiter: current status and future perspectives. Endocr. Rev. 24, 102–132 (2003). doi:10.1210/er.2002-0016

    Article  PubMed  Google Scholar 

  7. L. Leenhardt, P. Grosclaude, Epidemiology of thyroid carcinoma over the world. Ann. Endocrinol. 72, 136–138 (2011). doi:10.1016/j.ando.2011.03.025

    Article  CAS  Google Scholar 

  8. J. Rezzonico, M. Rezzonico, E. Pusiol, F. Pitoia, H. Niepomniszcze, Introducing the thyroid gland as another victim of the insulin resistance syndrome. Thyroid 18, 461–464 (2008). doi:10.1089/thy.2007.0223

    Article  CAS  PubMed  Google Scholar 

  9. F. Balkan, E.D. Onal, A. Usluogullari, D. Tuzun, D. Ozdemir, S.S. Inancli et al. Is there any association between insulin resistance and thyroid cancer? A case–control study. Endocrine 45, 55–60 (2014). doi:10.1007/s12020-013-9942-x

    Article  CAS  PubMed  Google Scholar 

  10. S.R. Shih, W.Y. Chiu, T.C. Chang, C.H. Tseng, Diabetes and thyroid cancer risk: literature review. Exp. Diabetes Res. 2012, 578285 (2012). doi:10.1155/2012/578285

    Article  PubMed  PubMed Central  Google Scholar 

  11. H. Guo, M. Sun, W. He, H. Chen, W. Li, J. Tang et al. The prevalence of thyroid nodules and its relationship with metabolic parameters in a Chinese community-based population aged over 40 years. Endocrine 45, 230–235 (2014). doi:10.1007/s12020-013-9968-0

    Article  CAS  PubMed  Google Scholar 

  12. M.A. Michalaki, A.G. Vagenakis, A.S. Leonardou, M.N. Argentou, I.G. Habeos, M.G. Makri et al.. Thyroid function in humans with morbid obesity. Thyroid 16, 73–78 (2006). doi:10.1089/thy.2006.16.73

    Article  CAS  PubMed  Google Scholar 

  13. C. Cappelli, I. Pirola, F. Mittempergher, E. De Martino, C. Casella, B. Agosti et al.. Morbid obesity in women is associated to a lower prevalence of thyroid nodules. Obes. Surg. 22, 460–464 (2012). doi:10.1007/s11695-011-0410-5

    Article  PubMed  Google Scholar 

  14. B. Biondi, Thyroid and obesity: an intriguing relationship. J. Clin. Endocrinol. Metab. 95, 3614–3617 (2010). doi:10.1210/jc.2010-1245

    Article  CAS  PubMed  Google Scholar 

  15. M. Finucane, G. Stevens, M. Cowan, G. Danaei, J.K. Lin, C.J. Paciorek et al.. National, regional and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet 377, 567–577 (2011). doi:10.1016/S0140-6736(10)62037-5

    Google Scholar 

  16. S.M. Grundy, Pre-diabetes, metabolic syndrome, and cardiovascular risk. J. Am. Coll. Cardiol. 59, 635–643 (2012). doi:10.1016/j.jacc.2011.08.080

    Article  CAS  PubMed  Google Scholar 

  17. S. Guth, U. Theune, J. Aberle, A. Galach, C.M. Bamberger, Very high prevalence of thyroid nodules detected by high frequency (13 MHz) ultrasound examination. Eur. J. Clin. Invest. 39, 699–706 (2009). doi:10.1111/j.1365-2362.2009.02162.x

    Article  CAS  PubMed  Google Scholar 

  18. C.S. Fox, M.J. Pencina, R.B. D’Agostino, J.M. Murabito, E.W. Seely, E.N. Pearce et al.. Relations of thyroid function to body weight: cross-sectional and longitudinal observations in a community-based sample. Arch. Intern. Med. 168, 587–592 (2008). doi:10.1001/archinte.168.6.587

    Article  PubMed  Google Scholar 

  19. N. Custro, V. Scafidi, M.C. De Francisci, S. Buscemi, Hormones of the pituitary-thyroid axis in obese subjects on free and low-calorie diet. Clin. Ther. 120, 199–203 (1987)

    CAS  Google Scholar 

  20. R. Parameswaran, S. Brooks, G.P. Sadler, Molecular pathogenesis of follicular cell derived thyroid cancers. Int. J. Surg. 8, 186–193 (2010). doi:10.1016/j.ijsu.2010.01.005

    Article  PubMed  Google Scholar 

  21. F. Delange, The disorders induced by iodine deficiency. Thyroid 4, 107–128 (1994). doi:10.1089/thy.1994.4.107

    Article  CAS  PubMed  Google Scholar 

  22. M. Andersson, V. Karumbunathan, M.B. Zimmermann, Global iodine status in 2011 and trends over the past decade. J. Nutr. 142, 744–750 (2012). doi:10.3945/jn.111.149393

    Article  CAS  PubMed  Google Scholar 

  23. R. Gutekunst, P.C. Scriba, Goiter and iodine deficiency in Europe. The European Thyroid Association report as updated in 1988. J. Endocrinol. Invest. 12, 209–220 (1989). doi:10.1007/BF03349967

    Article  CAS  PubMed  Google Scholar 

  24. S. Buscemi, A. Nicolucci, A. Mattina, G. Rosafio, F.M. Massenti, G. Lucisano et al. Association of dietary patterns with insulin resistance and clinically silent carotid atherosclerosis in apparently healthy people. Eur. J. Clin. Nutr. 67, 1284–1290 (2013). doi:10.1038/ejcn.2013.172

    Article  CAS  PubMed  Google Scholar 

  25. S. Buscemi, G. Rosafio, S. Vasto, F.M. Massenti, G. Grosso, F. Galvano et al. Validation of a food frequency questionnaire for use in Italian adults living in Sicily. Int. J. Food Sci. Nutr. 66, 426–438 (2015). doi:10.3109/09637486.2015.1025718

    Article  PubMed  Google Scholar 

  26. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 34(S1), S62–S69 (2011). doi:10.2337/dc11-S062

    Article  PubMed Central  Google Scholar 

  27. WHO. (2016). Obesity and overweight. http://apps.who.int/bmi/index.jsp?introPage=intro_3.html. Accessed 27th Jun 2017

  28. D.W. Kim, C.K. Eun, H.S. In, M.H. Kim, S.J. Jung, S.K. Bae, Sonographic differentiation of asymptomatic diffuse thyroid disease from normal thyroid: a prospective study. Am. J. Neuroradiol. 31, 1956–1960 (2010). doi:10.3174/ajnr.A2164

    Article  CAS  PubMed  Google Scholar 

  29. W.T. Friedewald, Estimation of the concentration of low density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18, 499–502 (1972)

    CAS  PubMed  Google Scholar 

  30. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and b-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419 (1985)

    Article  CAS  PubMed  Google Scholar 

  31. ISTAT. Statistiche demografiche Palermo. http://www.tuttitalia.it/sicilia/81-palermo/statistiche/popolazione-eta-sesso-stato-civile-2015. Accessed 18 Dec 2015

  32. S. Buscemi, G. Geraci, F.M. Massenti, C. Buscemi, F. Costa, C. D’Orio, G. Rosafio, C. Buscemi, V. Maniaci, G. Parrinello, Renal function and carotid atherosclerosis in adults with no known kidney disease. Nutr. Metab. Cardiovasc. Dis. 27, 267–273 (2017). doi:10.1016/j.numecd.2016.09.013

    Article  CAS  PubMed  Google Scholar 

  33. N. Knudsen, I. Bülow, T. Jorgensen, P. Laurberg, L. Ovesen, H. Perrild, Goitre prevalence and thyroid abnormalities at ultrasonography: a comparative epidemiological study in two regions with slightly different iodine status. Clin. Endocrinol. 53, 479–485 (2000)

    Article  CAS  Google Scholar 

  34. Corsaro, L., Falco, V., Venturi, F., Dotta, F., Frontoni, S., Lauro, D., et al. (2015). Analysis of the diabetes in Italy. The Italian Barometer Diabetes Observatory. http://www.ibdo.it/pdf/diabetesmonitor2015n2.pdf. Accessed 30 Dec 2015

  35. ISTAT. Obesità e sovrappeso. http://www3.istat.it/salastampa/comunicati/non_calendario/20010313_00/. Accessed 30 Dec 2015

  36. S. Ezzat, D.A. Sarti, D.R. Cain, G.D. Braunstein, Thyroid incidentalomas. Prevalence by palpation and ultrasonography. Arch. Intern. Med. 154, 1838–1840 (1994)

    Article  CAS  PubMed  Google Scholar 

  37. G. Panagiotou, D. Komninou, P. Anagnostis, G. Linardos, E. Karoglou, M. Somali et al. Association between lifestyle and anthropometric parameters and thyroid nodule features. Endocrine 56, 560–567 (2017). doi:10.1007/s12020-017-1285-6

    Article  CAS  PubMed  Google Scholar 

  38. B.S. Hetzel, J.T. Dunn, The iodine deficiency disorders: their nature and prevention. Annu. Rev. Nutr. 9, 21–38 (1989). doi:10.1146/annurev.nu.09.070189.000321

    Article  CAS  PubMed  Google Scholar 

  39. Buscemi, S., Nicolucci, A., Lucisano, G., Mattina, A., Rosafio, G., Barile, A.M., et al. (2014). Stile di vita e prevalenza di obesità, ipertensione e diabete in un campione di bambini, adolescenti e adulti. Lo studio ABCD. Proceedings of the 25th National Congress of the Italian Society of Diabetology, Bologna

  40. V.F. Brauer, W.H. Brauer, D. Führer, R. Paschke, Iodine nutrition, nodular thyroid disease, and urinary iodine excretion in a German university study population. Thyroid 15, 364–370 (2005). doi:10.1089/thy.2005.15.364

    Article  CAS  PubMed  Google Scholar 

  41. L. Dahl, L. Johansson, K. Julshamn, H.M. Meltzer, The iodine content of Norwegian foods and diets. Public Health Nutr. 7, 569–576 (2004). doi:10.1079/PHN2003554

    Article  PubMed  Google Scholar 

  42. F. Soriguer, E. Garcia-Fuentes, C. Gutierrez-Repiso, G. Rojo-Martinez, I. Velasco et al. Iodine intake in the adult population. Di@bet.es study. Clin. Nutr. 31, 882–888 (2012). doi:10.1016/j.clnu.2012.04.004

    Article  CAS  PubMed  Google Scholar 

  43. Z. Chen, W. Xu, Y. Huang, X. Jin, J. Deng, S. Zhu et al.. Associations of noniodized salt and thyroid nodule among the Chinese population: a large cross-sectional study. Am. J. Clin. Nutr. 98, 684–692 (2013). doi:10.3945/ajcn.112.054353

    Article  CAS  PubMed  Google Scholar 

  44. L.B. Rasmussen, L. Ovesen, I. Bülow, T. Jørgensen, N. Knudsen, P. Laurberg et al. Relations between various measures of iodine intake and thyroid volume, thyroid nodularity, and serum thyroglobulin. Am. J. Clin. Nutr. 76, 1069–1076 (2002)

    Article  CAS  PubMed  Google Scholar 

  45. G.R. Burgio, G. Flatz, C. Barbera, R. Patané, A. Boner, C. Cajozzo et al. Prevalence of primary adult lactose malabsorption and awareness of milk intolerance in Italy. Am, J. Clin. Nutr. 39, 100–104 (1984)

    Article  CAS  Google Scholar 

  46. T. Mijović, J. How, M. Pakdaman, L. Rochon, O. Gologan, M.P. Hier et al. Body mass index in the evaluation of thyroid cancer risk. Thyroid 19, 467–472 (2009). doi:10.1089/thy.2008.0386

    Article  PubMed  Google Scholar 

  47. L. Scappaticcio, M.I. Maiorino, G. Bellastella, D. Giugliano, K. Esposito, Insights into the relationships between diabetes, prediabetes, and cancer. Endocrine 56, 231–239 (2017). doi:10.1007/s12020-016-1216-y

    Article  CAS  PubMed  Google Scholar 

  48. F. Pitoia, E. Abelleira, F. Bueno, C. Urciuoli, A. Schmidt, H. Niepomniszcze, Insulin resistance is another factor that increases the risk of recurrence in patients with thyroid cancer. Endocrine 48, 894–901 (2015). doi:10.1007/s12020-014-0416-6

    Article  CAS  PubMed  Google Scholar 

  49. US Preventive Services Task Force. Screening for thyroid cancer: US preventive services task force recommendation statement. JAMA 317, 1882–1887 (2017). doi:10.1001/jama.2017.4011

    Article  Google Scholar 

  50. O.M. Pedersen, N.P. Aardal, T.B. Larssen, J.E. Varhaug, O. Myking, H. Vik-Mo, The value of ultrasonography in predicting autoimmune thyroid disease. Thyroid 10, 251–259 (2000). doi:10.1089/thy.2000.10.251

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento Biomedico di Medicina Interna e Specialistica (DIBIMIS) – University of Palermo (Italy), Via del Vespro 129, 90127, Palermo, Italy

    Silvio Buscemi, Carola Buscemi, Davide Corleo, Anna Maria Barile, Giuseppe Rosafio, Nadia Rini & Carla Giordano

  2. Laboratorio di Metabolismo e Nutrizione Clinica – AOU Policlinico “P. Giaccone”, Palermo, Italy

    Silvio Buscemi, Carola Buscemi, Davide Corleo, Anna Maria Barile, Giuseppe Rosafio & Nadia Rini

  3. Dipartimento di Scienze per la Promozione della Salute e Materno Infantile – University of Palermo, (Italy) - AOU Policlinico “P. Giaccone”, Palermo, Italy

    Fatima Maria Massenti

  4. Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche (STEBICEF), University of Palermo (Italy), Palermo, Italy

    Sonya Vasto

  5. Dipartimento di Scienze del Farmaco, University of Catania (Italy), Catania, Italy

    Fabio Galvano

  6. Sezione di Malattie Cardio-Respiratorie ed Endocrino-Metaboliche, Roma, Italy

    Carla Giordano

Authors
  1. Silvio Buscemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatima Maria Massenti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonya Vasto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabio Galvano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carola Buscemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Davide Corleo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anna Maria Barile
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Giuseppe Rosafio
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nadia Rini
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Carla Giordano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Silvio Buscemi.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all participants included in the study.

Appendix

Appendix

Table 4

Table 4 Demographic characteristics of the ABCD cohort compared with those of the general population living in Palermo
Full size table

and Table 5

Table 5 Characteristics of the cohort divided according to the presence of thyroid nodules
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buscemi, S., Massenti, F.M., Vasto, S. et al. Association of obesity and diabetes with thyroid nodules. Endocrine 60, 339–347 (2018). https://doi.org/10.1007/s12020-017-1394-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-017-1394-2

Keywords

Search

Navigation