Advertisement

Hormones

, Volume 17, Issue 4, pp 565–571 | Cite as

Iodine intake and chronic autoimmune thyroiditis: a comparative study between coastal and mainland regions in Greece

  • Τ. Giassa
  • I. Mamali
  • Ε. Gaki
  • G. Kaltsas
  • G. Kouraklis
  • Κ. Β. MarkouEmail author
  • T. Karatzas
Original Article

Abstract

Introduction

The purpose of this study was to evaluate the relationship between iodine intake and autoimmune thyroiditis in Chios, an island located in the North East Aegean Sea, in comparison to mainland regions in South Western Greece (SWG).

Materials and methods

Urine iodine concentration (UIC), thyroid function (serum TSH, thyroid autoantibodies: anti-TPO and anti-Tg), and thyroid U/S were assessed in 200 subjects (150 females and 50 males) from Chios and 322 subjects (255 females and 67 males) from several mainland regions in SWG. All participants were recruited from outpatient clinics and were diagnosed as euthyroid.

Results

Median UIC in Chios was significantly higher compared to SWG (136.1 vs. 104.5 μg/L, p < 0.001), indicating that both regions are iodine sufficient according to World Health Organization (WHO) criteria. The prevalence of thyroid autoimmunity was 66.5% in Chios and 27% in SWG, significantly higher in females (46.7%) than in males (26.5%). Furthermore, individuals with increased levels of thyroid autoantibodies either anti-TPO or anti-Tg (TAbs) showed increased median UIC levels compared to those / subjects / patients with normal levels (126.7 vs. 108.95 μg/L, p < 0.001). Serum TSH mean values (mIU/L) were greater in females (mean = 2.1 ± 1.41) compared to males (mean = 1.82 ± 1.26) (p = 0.04) and decreased with age.

Conclusions

In conclusion, in the present study, we clearly indicate that increased thyroid autoimmunity is positively associated with increased iodine intake, as well as with the female gender. Moreover, iodine intake and thyroid autoimmunity appear to be significantly higher in a coastal region (Chios) than in mainland Greece (SWG). Additional environmental factors, apart from iodine, should be investigated in future studies. Mean TSH values were increased in females and decreased with age. The latter is probably due to the presence of autonomous goiter in older Greek populations, as a result of long-term status of iodine deficiency in the past.

Keywords

Iodine Autoimmune thyroid disease Thyroiditis Thyroid Greece 

Notes

Compliance with ethical standards

This comparative prospective study was approved by the Ethical committee of University Hospital of Patras in Greece and patient consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    WHO (2007) Assessment of iodine deficiency disorders and monitoring their elimination: a guide for programme managers, 3rd edn. WHO, SwitzerlandGoogle Scholar
  2. 2.
    Zimmermann MB (2009) Iodine deficiency. Endocr Rev 30(4):376–408PubMedPubMedCentralGoogle Scholar
  3. 3.
    Laurberg P, Cerqueira C, Ovesen L, Rasmussen LB, Perrild H, Andersen S, Pedersen IB, Carle A (2010) Iodine intake as a determinant of thyroid disorders in populations. Best Pract Res Clin Endocrinol Metab 24(1):13–27PubMedGoogle Scholar
  4. 4.
    de Escobar GM, Obregon MJ, del Rey FE (2007) Iodine deficiency and brain development in the first half of pregnancy. Public Health Nutr 10(12A):1554–1570PubMedGoogle Scholar
  5. 5.
    Markou KB, Koukkou EG (2012) The Greek population is iodine sufficient and not at risk of iodine-induced hyperthyroidism. J Nutr 142(8):1611 author reply 1612PubMedGoogle Scholar
  6. 6.
    Koukkou EG, Roupas ND, Markou KB (2017) Effect of excess iodine intake on thyroid on human health. Minerva Med 108(2):136–146PubMedGoogle Scholar
  7. 7.
    Pearce EN (2015) Thyroid disorders during pregnancy and postpartum. Best Pract Res Clin Obstet Gynaecol 29(5):700–706PubMedPubMedCentralGoogle Scholar
  8. 8.
    McGrogan A, Seaman HE, Wright JW, de Vries CS (2008) The incidence of autoimmune thyroid disease: a systematic review of the literature. Clin Endocrinol 69(5):687–696Google Scholar
  9. 9.
    Root-Bernstein R, Fairweather D (2014) Complexities in the relationship between infection and autoimmunity. Curr Allergy Asthma Rep 14(1):407PubMedPubMedCentralGoogle Scholar
  10. 10.
    Saeki Y, Ishihara K (2014) Infection-immunity liaison: pathogen-driven autoimmune-mimicry (PDAIM). Autoimmun Rev 13(10):1064–1069PubMedGoogle Scholar
  11. 11.
    Lee HJ, Li CW, Hammerstad SS, Stefan M, Tomer Y (2015) Immunogenetics of autoimmune thyroid diseases: a comprehensive review. J Autoimmun 64:82–90PubMedPubMedCentralGoogle Scholar
  12. 12.
    Medici M, Porcu E, Pistis G, Teumer A, Brown SJ, Jensen RA, Rawal R, Roef GL, Plantinga TS, Vermeulen SH, Lahti J, Simmonds MJ, Husemoen LL, Freathy RM, Shields BM, Pietzner D, Nagy R, Broer L, Chaker L, Korevaar TI, Plia MG, Sala C, Volker U, Richards JB, Sweep FC, Gieger C, Corre T, Kajantie E, Thuesen B, Taes YE, Visser WE, Hattersley AT, Kratzsch J, Hamilton A, Li W, Homuth G, Lobina M, Mariotti S, Soranzo N, Cocca M, Nauck M, Spielhagen C, Ross A, Arnold A, van de Bunt M, Liyanarachchi S, Heier M, Grabe HJ, Masciullo C, Galesloot TE, Lim EM, Reischl E, Leedman PJ, Lai S, Delitala A, Bremner AP, Philips DI, Beilby JP, Mulas A, Vocale M, Abecasis G, Forsen T, James A, Widen E, Hui J, Prokisch H, Rietzschel EE, Palotie A, Feddema P, Fletcher SJ, Schramm K, Rotter JI, Kluttig A, Radke D, Traglia M, Surdulescu GL, He H, Franklyn JA, Tiller D, Vaidya B, de Meyer T, Jorgensen T, Eriksson JG, O'Leary PC, Wichmann E, Hermus AR, Psaty BM, Ittermann T, Hofman A, Bosi E, Schlessinger D, Wallaschofski H, Pirastu N, Aulchenko YS, de la Chapelle A, Netea-Maier RT, Gough SC, Meyer Zu Schwabedissen H, Frayling TM, Kaufman JM, Linneberg A, Raikkonen K, Smit JW, Kiemeney LA, Rivadeneira F, Uitterlinden AG, Walsh JP, Meisinger C, den Heijer M, Visser TJ, Spector TD, Wilson SG, Volzke H, Cappola A, Toniolo D, Sanna S, Naitza S, Peeters RP (2014) Identification of novel genetic loci associated with thyroid peroxidase antibodies and clinical thyroid disease. PLoS Genet 10(2):e1004123PubMedPubMedCentralGoogle Scholar
  13. 13.
    Tomer Y (2014) Mechanisms of autoimmune thyroid diseases: from genetics to epigenetics. Annu Rev Pathol 9:147–156PubMedPubMedCentralGoogle Scholar
  14. 14.
    Bogdanos DP, Smyk DS, Invernizzi P, Rigopoulou EI, Blank M, Pouria S, Shoenfeld Y (2013) Infectome: a platform to trace infectious triggers of autoimmunity. Autoimmun Rev 12(7):726–740PubMedGoogle Scholar
  15. 15.
    Duntas LH (2011) Environmental factors and thyroid autoimmunity. Ann Endocrinol (Paris) 72(2):108–113Google Scholar
  16. 16.
    Burek CL, Talor MV (2009) Environmental triggers of autoimmune thyroiditis. J Autoimmun 33(3–4):183–189PubMedPubMedCentralGoogle Scholar
  17. 17.
    Hansen PS, Brix TH, Iachine I, Kyvik KO, Hegedus L (2006) The relative importance of genetic and environmental effects for the early stages of thyroid autoimmunity: a study of healthy Danish twins. Eur J Endocrinol 154(1):29–38PubMedGoogle Scholar
  18. 18.
    Pani F, Atzori F, Baghino G, Boi F, Tanca L, Ionta MT, Mariotti S (2015) Thyroid dysfunction in patients with metastatic carcinoma treated with sunitinib: is thyroid autoimmunity involved? Thyroid 25(11):1255–1261PubMedGoogle Scholar
  19. 19.
    Tomer Y, Blackard JT, Akeno N (2007) Interferon alpha treatment and thyroid dysfunction. Endocrinol Metab Clin N Am 36 (4):1051–1066; x-xiGoogle Scholar
  20. 20.
    Benvenga S, Guarneri F (2016) Molecular mimicry and autoimmune thyroid disease. Rev Endocr Metab Disord 17(4):485–498PubMedGoogle Scholar
  21. 21.
    Guastamacchia E, Giagulli VA, Licchelli B, Triggiani V (2015) Selenium and iodine in autoimmune thyroiditis. Endocr Metab Immune Disord Drug Targets 15(4):288–292PubMedPubMedCentralGoogle Scholar
  22. 22.
    Tomer Y, Huber A (2009) The etiology of autoimmune thyroid disease: a story of genes and environment. J Autoimmun 32(3–4):231–239PubMedPubMedCentralGoogle Scholar
  23. 23.
    Dunn JT, Crutchfield HE, Gutekunst R, Dunn AD (1993) Two simple methods for measuring iodine in urine. Thyroid 3(2):119–123PubMedGoogle Scholar
  24. 24.
    Gutekunst R, Hafermann W, Mansky T, Scriba PC (1989) Ultrasonography related to clinical and laboratory findings in lymphocytic thyroiditis. Acta Endocrinol 121(1):129–135PubMedGoogle Scholar
  25. 25.
    Markou K, Michalaki M, Makri M, Georgopoulos N, Pagoni C, Sorras K, Alexandrides T, Kyriazopoulou V, Vagenakis AG (1996) Iodine intake and thyroid function in villagers and city dwellers in southwestern Greece. Thyroid 1 (Suppl):S79Google Scholar
  26. 26.
    Michalaki M, Kyriazopoulou V, Paraskevopoulou P, Vagenakis AG, Markou KB (2008) The odyssey of nontoxic nodular goiter (NTNG) in Greece under suppression therapy, and after improvement of iodine deficiency. Thyroid 18(6):641–645PubMedGoogle Scholar
  27. 27.
    Koukkou EG, Ilias I, Mamalis I, Markou KB (2016) Pregnant Greek women may have a higher prevalence of iodine deficiency than the general Greek population. Eur Thyroid J 6(1):26–30PubMedPubMedCentralGoogle Scholar
  28. 28.
    Koutras DA, Alevizaki M, Tsatsoulis A, Vagenakis AG (2003) Greece is iodine sufficient. Lancet 362(9381):405–406PubMedGoogle Scholar
  29. 29.
    Doufas AG, Mastorakos G, Chatziioannou S, Tseleni-Balafouta S, Piperingos G, Boukis MA, Mantzos E, Caraiskos CS, Mantzos J, Alevizaki M, Koutras DA (1999) The predominant form of non-toxic goiter in Greece is now autoimmune thyroiditis. Eur J Endocrinol 140(6):505–511PubMedGoogle Scholar
  30. 30.
    Zois C, Stavrou I, Kalogera C, Svarna E, Dimoliatis I, Seferiadis K, Tsatsoulis A (2003) High prevalence of autoimmune thyroiditis in schoolchildren after elimination of iodine deficiency in northwestern Greece. Thyroid 13(5):485–489PubMedGoogle Scholar
  31. 31.
    Pearce EN, Alexiou M, Koukkou E, Braverman LE, He X, Ilias I, Alevizaki M, Markou KB (2012) Perchlorate and thiocyanate exposure and thyroid function in first-trimester pregnant women from Greece. Clin Endocrinol 77(3):471–474Google Scholar
  32. 32.
    Smyth PP, Burns R, Huang RJ, Hoffman T, Mullan K, Graham U, Seitz K, Platt U, O'Dowd C (2011) Does iodine gas released from seaweed contribute to dietary iodine intake? Environ Geochem Health 33(4):389–397PubMedGoogle Scholar
  33. 33.
    Smyth P, Burns R, Casey M, Mullan K, O'Herlihy C, O'Dowd C (2016) Iodine status over two decades: influence of seaweed exposure. Ir Med J 109(6):421PubMedGoogle Scholar
  34. 34.
    Westby T, Cadogan A, Duignan G (2018) In vivo uptake of iodine from a Fucus serratus Linnaeus seaweed bath: does volatile iodine contribute? Environ Geochem Health 40(2):683–691PubMedGoogle Scholar
  35. 35.
    Pedersen IB, Knudsen N, Jorgensen T, Perrild H, Ovesen L, Laurberg P (2003) Thyroid peroxidase and thyroglobulin autoantibodies in a large survey of populations with mild and moderate iodine deficiency. Clin Endocrinol 58(1):36–42Google Scholar
  36. 36.
    Boukis MA, Koutras DA, Souvatzoglou A, Evangelopoulou A, Vrontakis M, Moulopoulos SD (1983) Thyroid hormone and immunological studies in endemic goiter. J Clin Endocrinol Metab 57(4):859–862PubMedPubMedCentralGoogle Scholar
  37. 37.
    Latrofa F, Fiore E, Rago T, Antonangeli L, Montanelli L, Ricci D, Provenzale MA, Scutari M, Frigeri M, Tonacchera M, Vitti P (2013) Iodine contributes to thyroid autoimmunity in humans by unmasking a cryptic epitope on thyroglobulin. J Clin Endocrinol Metab 98(11):E1768–E1774PubMedPubMedCentralGoogle Scholar
  38. 38.
    Laurberg P, Bulow Pedersen I, Knudsen N, Ovesen L, Andersen S (2001) Environmental iodine intake affects the type of nonmalignant thyroid disease. Thyroid 11(5):457–469PubMedPubMedCentralGoogle Scholar
  39. 39.
    Laurberg P, Pedersen KM, Hreidarsson A, Sigfusson N, Iversen E, Knudsen PR (1998) Iodine intake and the pattern of thyroid disorders: a comparative epidemiological study of thyroid abnormalities in the elderly in Iceland and in Jutland, Denmark. J Clin Endocrinol Metab 83(3):765–769PubMedPubMedCentralGoogle Scholar
  40. 40.
    Pedersen IB, Knudsen N, Carle A, Vejbjerg P, Jorgensen T, Perrild H, Ovesen L, Rasmussen LB, Laurberg P (2011) A cautious iodization programme bringing iodine intake to a low recommended level is associated with an increase in the prevalence of thyroid autoantibodies in the population. Clin Endocrinol 75(1):120–126Google Scholar
  41. 41.
    Vanderpump MP (2011) The epidemiology of thyroid disease. Br Med Bull 99:39–51PubMedPubMedCentralGoogle Scholar
  42. 42.
    Vanderpump MP, Tunbridge WM, French JM, Appleton D, Bates D, Clark F, Grimley Evans J, Hasan DM, Rodgers H, Tunbridge F et al (1995) The incidence of thyroid disorders in the community: a twenty-year follow-up of the Whickham survey. Clin Endocrinol 43(1):55–68Google Scholar
  43. 43.
    Vanderpump MPJ (2005) The epidemiology of thyroid diseases. In: Braverman LE, Utiger RD (eds) Werner and Ingbar’s the thyroid: a fundamental and clinical text, 9th edn. JB. Lippincott-Raven, Philadelphia, pp 398–496Google Scholar
  44. 44.
    Eschler DC, Hasham A, Tomer Y (2011) Cutting edge: the etiology of autoimmune thyroid diseases. Clin Rev Allergy Immunol 41(2):190–197PubMedPubMedCentralGoogle Scholar
  45. 45.
    Brent GA (2010) Environmental exposures and autoimmune thyroid disease. Thyroid 20(7):755–761PubMedPubMedCentralGoogle Scholar
  46. 46.
    Papanastasiou L, Vatalas IA, Koutras DA, Mastorakos G (2007) Thyroid autoimmunity in the current iodine environment. Thyroid 17(8):729–739PubMedGoogle Scholar
  47. 47.
    Mooij P, Simons PJ, de Haan-Meulman M, de Wit HJ, Drexhage HA (1994) Effect of thyroid hormones and other iodinated compounds on the transition of monocytes into veiled/dendritic cells: role of granulocyte-macrophage colony-stimulating factor, tumour-necrosis factor-alpha and interleukin-6. J Endocrinol 140(3):503–512PubMedGoogle Scholar
  48. 48.
    Carayanniotis G, Rao VP (1997) Searching for pathogenic epitopes in thyroglobulin: parameters and caveats. Immunol Today 18(2):83–88PubMedGoogle Scholar
  49. 49.
    Rasooly L, Rose NR, Saboori AM, Ladenson PW, Burek CL (1998) Iodine is essential for human T cell recognition of human thyroglobulin. Autoimmunity 27(4):213–219PubMedGoogle Scholar
  50. 50.
    Many MC, Maniratunga S, Varis I, Dardenne M, Drexhage HA, Denef JF (1995) Two-step development of Hashimoto-like thyroiditis in genetically autoimmune prone non-obese diabetic mice: effects of iodine-induced cell necrosis. J Endocrinol 147(2):311–320PubMedGoogle Scholar
  51. 51.
    Many MC, Mestdagh C, van den Hove MF, Denef JF (1992) In vitro study of acute toxic effects of high iodide doses in human thyroid follicles. Endocrinology 131(2):621–630PubMedGoogle Scholar
  52. 52.
    Huang CJ, Tseng CL, Chen HS, Garabwan C, Korovo S, Tang KT, Won JG, Hsieh CH, Wang FF (2016) Iodine nutritional status of school children in Nauru 2015. Nutrients 8(9)Google Scholar
  53. 53.
    Madar AA, Meltzer HM, Heen E, Meyer HE (2018) Iodine status among Somali immigrants in Norway. Nutrients 10(3)Google Scholar
  54. 54.
    Hollowell JG, Staehling NW, Flanders WD, Hannon WH, Gunter EW, Spencer CA, Braverman LE (2002) Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab 87(2):489–499PubMedPubMedCentralGoogle Scholar
  55. 55.
    Vadiveloo T, Donnan PT, Murphy MJ, Leese GP (2013) Age- and gender-specific TSH reference intervals in people with no obvious thyroid disease in Tayside, Scotland: the Thyroid Epidemiology, Audit, and Research Study (TEARS). J Clin Endocrinol Metab 98(3):1147–1153PubMedPubMedCentralGoogle Scholar
  56. 56.
    van de Ven AC, Netea-Maier RT, Smit JW, Kusters R, van der Stappen JW, Pronk-Admiraal CJ, Buijs MM, Schoenmakers CH, Koehorst SG, de Groot MJ, Sweep FC, Hermus AR, den Heijer M (2015) Thyrotropin versus age relation as an indicator of historical iodine intake. Thyroid 25(6):629–634PubMedGoogle Scholar
  57. 57.
    Dayan CM, Daniels GH (1996) Chronic autoimmune thyroiditis. N Engl J Med 335(2):99–107PubMedGoogle Scholar
  58. 58.
    Tomer Y (1997) Anti-thyroglobulin autoantibodies in autoimmune thyroid diseases: cross-reactive or pathogenic? Clin Immunol Immunopathol 82(1):3–11PubMedGoogle Scholar
  59. 59.
    Papageorgiou VPB-CM, Apazidou KK, Psarros EE (1997) Gas chromatographic–mass spectroscopic analysis of the acidic triterpenic fraction of mastic gum. J Chromatogr A 769(2):263–273Google Scholar
  60. 60.
    Magiatis P, Melliou E, Skaltsounis AL, Chinou IB, Mitaku S (1999) Chemical composition and antimicrobial activity of the essential oils of Pistacia lentiscus var. chia. Planta Med 65(8):749–752PubMedGoogle Scholar
  61. 61.
    Chandra AK, Mondal C, Sinha S, Chakraborty A, Pearce EN (2015) Synergic actions of polyphenols and cyanogens of peanut seed coat (Arachis hypogaea) on cytological, biochemical and functional changes in thyroid. Indian J Exp Biol 53(3):143–151PubMedGoogle Scholar
  62. 62.
    Chandra AK, De N (2010) Goitrogenic/antithyroidal potential of green tea extract in relation to catechin in rats. Food Chem Toxicol 48(8–9):2304–2311PubMedGoogle Scholar

Copyright information

© Hellenic Endocrine Society 2018

Authors and Affiliations

  • Τ. Giassa
    • 1
  • I. Mamali
    • 1
  • Ε. Gaki
    • 2
  • G. Kaltsas
    • 3
  • G. Kouraklis
    • 3
  • Κ. Β. Markou
    • 1
    Email author
  • T. Karatzas
    • 3
  1. 1.Department of Internal Medicine, Division of EndocrinologyUniversity of Patras Medical School, University HospitalRionGreece
  2. 2.Department of Business AdministrationUniversity of the AegeanLesbosGreece
  3. 3.Laikon General HospitalNational and Kapodistrian University of AthensAthensGreece

Personalised recommendations