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The Environment and Autoimmune Thyroid Diseases

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The Environment and Autoimmune Thyroid Diseases European Journal of Endocrinology (2004) 150 605–618 ISSN 0804-4643 INVITED REVIEW The environment and autoimmune thyroid diseases Mark F Prummel, Thea Strieder and Wilmar M Wiersinga Department of Endocrinology and Metabolism, F5-171, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands (Correspondence should be addressed to M F Prummel; Email: [email protected]) Abstract Genetic factors play an important role in the pathogenesis of autoimmune thyroid disease (AITD) and it has been calculated that 80% of the susceptibility to develop Graves’ disease is attributable to genes. The concordance rate for AITD among monozygotic twins is, however, well below 1 and environmen- tal factors thus must play an important role. We have attempted to carry out a comprehensive review of all the environmental and hormonal risk factors thought to bring about AITD in genetically pre- disposed individuals. Low birth weight, iodine excess and deficiency, selenium deficiency, parity, oral contraceptive use, reproductive span, fetal microchimerism, stress, seasonal variation, allergy, smok- ing, radiation damage to the thyroid gland, viral and bacterial infections all play a role in the development of autoimmune thyroid disorders. The use of certain drugs (lithium, interferon-a, Cam- path-1H) also increases the risk of the development of autoimmunity against the thyroid gland. Further research is warranted into the importance of fetal microchimerism and of viral infections capable of mounting an endogenous interferon-a response. European Journal of Endocrinology 150 605–618 Introduction Graves’ disease and Hashimoto’s thyroiditis. Despite their different phenotype, they do share some hom- Graves’ hyperthyroidism, Hashimoto’s hypothyroidism ology. First, autoantibodies against thyroid peroxidase and post-partum thyroid dysfunction are common dis- (TPO) are common in both diseases. Secondly, Graves’ orders. They have an autoimmune origin and are there- disease and Hashimoto’s thyroiditis appear to run in fore also alluded to as autoimmune thyroid disease the same families and thus share a common genetic (AITD). Like other organ-specific autoimmune endocri- background (7, 8). nopathies, e.g. type I diabetes mellitus (IDDM), they have a multifactorial etiology. Genes are certainly involved and in order to develop AITD a subject will Fetal growth have a certain genetic susceptibility, probably involving multiple genes of which only a few have been identified. Reduced fetal growth is a risk factor for several common Most notably, certain human leukocyte antigen (HLA)- disorders, such as chronic heart disease (9), and famine DR genes determine this genetic susceptibility, but there exposure during fetal life is associated with subsequent are other genes involved and AITD thus has a polygenetic glucose intolerance during adult life (10). Prenatal mal- background. Nevertheless, non-genetic (environmental, nutrition is associated with a lower thymic and splenic hormonal) factors must also play an important etiologic weight (11), and this may cause earlier maturation of role, because the concordance rate for AITD in monozy- the thymus resulting in a decline in T suppressor cells gotic twins is not 100%. Another argument is that immi- (12). Indeed, Phillips et al. (12) found that among 305 grants coming from countries with a low incidence of women aged 60–71 years born in the UK the presence autoimmune diseases will adopt the incidence rate of of TPO antibodies was positively related to lower birth the new country. For instance, type I diabetes mellitus weights (but not to weight at 1 year of age). The preva- is 10 times more frequent in Pakistanis living in the UK lence of TPO antibodies was 2.4 times higher in than in those living in Pakistan (1). women with a birth weight of less than 5.5 lbs In recent years, a number of excellent reviews have (2.49 kg) compared with those with a higher birth been published on the genetic background of AITD weight. In a twin study, the same group found that (2–6). Here we will attempt to review the environmen- among monozygous twins, the smaller twin had higher tal factors that may be involved in the development of levels of TPO antibodies (13). Because of the genetic iden- AITD (Table 1). In this review we will consider both tity of monozygous twins, this study strongly suggests q 2004 Society of the European Journal of Endocrinology Online version via http://www.eje.org Downloaded from Bioscientifica.com at 09/26/2021 12:16:14AM via free access 606 M F Prummel and others EUROPEAN JOURNAL OF ENDOCRINOLOGY (2004) 150 Table 1 Environmental factors involved in the etiology of AITD. Environmental factor Mechanism Phenotype Low birth weight Insufficient thymic maturation TPO antibodies Iodine excess No escape from Wolff–Chaikoff effect HT Jod-Basedow GD Selenium deficiency Unknown; viral infections? HT Longer reproductive span Estradiol effect? HT Oral contraceptives Protective TPO antibodies Fetal michrochimerism Male cells in thyroid elicit antithyroid attack HT and GD Stress Upregulation HPA axis GD Allergy Unknown; high IgE levels GD Smoking Hypoxia? High IgE levels GD; esp. GO Yersinia enterocolitica Molecular mimicry GD infection See text for explanation and references. GD, Graves’ disease; HT, Hashimoto’s thyroiditis; GO, Graves’ ophthalmopathy. that certain intrauterine factors causing reduced fetal amino acid. It is incorporated into 35 selenoproteins, growth are the first environmental risk factors for mostly enzymes (26). Selenium also has a marked influ- AITD in later life. However, this was not confirmed in ence on the immune system and selenium deficiency is another twin study where birth weight was not found associated with a greater susceptibility for viral infec- to be a determinant for clinically overt AITD (14). tions such as the Coxsackie virus (27), possibly because T-lymphocytes have an important functional need for selenium (26). In addition, selenium acts as an anti- Iodine intake oxidant and reduces free radical formation. It plays an essential role in thyroid hormone synthesis, because Iodine intake seems to influence the prevalence rates of two enzymes involved in thyroid hormone production hyper- and hypothyroidism. In areas with sufficient are selenoproteins: the deiodinases and glutathione per- iodine intake, hypothyroidism is more common than oxidase (28). Selenium deficiency leads to a variety of in iodine-deficient regions (15), whereas the overall symptoms including a higher miscarriage rate (29) prevalence of thyrotoxicosis is greater in iodine- and a higher cancer mortality rate (26). deficient areas (16). Looking at the different causes of Selenium intake in Europe is lower than in the hyperthyroidism, Graves’ hyperthyroidism as the United States and in many countries it is below the cause of thyrotoxicosis is seen more frequently in UK reference nutrient intake of 75 mg/day. Sources of iodine-replete areas (17), and TPO antibodies as a selenium are crab, other shellfish and fish, but alterna- marker for impending thyroid failure are more preva- tive sources such as wheat are relatively low in sel- lent in iodine-deficient regions (18). enium content because of the low selenium Excessive iodine intake can cause dysthyroidism, availability in European soils (26). especially in patients with underlying autoimmune thy- Low selenium blood levels are associated with roiditis (19). Due to a failure to escape from the Wolff– increased thyroid volume and with thyroid hypoecho- Chaikoff effect, iodine excess can cause hypothyroidism genicity, a marker for lymphocytic infiltration (30). In and/or goiter, but if autonomously functioning nodules agreement with this finding, a recent double-blind ran- or a subclinical form of Graves’ disease are present, it domized trial in patients with subclinical hypothryoid- can also induce hyperthyroidism (Jod–Basedow effect) ism showed that treatment with 200 mg sodium (20, 21). Both phenomena are thought to lead to selenite caused a significant decrease in TPO antibody some thyroid destruction and hence presentation of titers (as well as an increase in quality of life), without thyroidal antigens to the immune system leading to affecting thyroid hormone status (31). In another an autoimmune reaction (22). It thus appears that randomized trial in patients with subclinical hypo- iodine intake is indeed a risk factor for the development thyroidism who were treated with thyroxine supple- of AITD. This is in agreement with animal studies mentation, addition of 200 mg selenium methionine showing that a high iodine intake aggravates auto- led to a significant decrease in TPO antibody concen- immune thyroiditis in several genetically susceptible trations (32). animal strains (23–25). Hormonal influences: female sex Selenium intake One of the most striking characteristics of organ- Selenium is a trace mineral and an essential nutrient specific autoimmune diseases is its female preponder- for selenocysteine synthesis and is also called the 21st ance. The female:male ratio for Graves’ disease and www.eje.org Downloaded from Bioscientifica.com at 09/26/2021 12:16:14AM via free access EUROPEAN JOURNAL OF ENDOCRINOLOGY (2004) 150 The environment and autoimmune thyroid diseases 607 Hashimoto’s thyroiditis is 5–10:1 (33). The reason for be associated with either subclinical hypothyroidism this is unclear and genetic factors must play a role, or the presence of TPO antibodies (39), although in although it is noteworthy that Hashimoto’s thyroiditis one case report an exacerbation of eye symptoms was is very prevalent among girls with Turner’s syndrome seen in a woman with Graves’ ophthalmopathy starting (XO karyotype), but not in men with Klinefelter’s syn- HRT (40). As for oral contraceptives, used by over 100 drome (XXY karyotype) (6). The influence of the X million women worldwide (41), there are remarkably chromosome is thus limited and hormonal influences few studies on their use and the development of AITD may also be operative in the induction of AITD. It is and in contrast to what one intuitively may think interesting to note the female preponderance in non- their use seems to protect against AITD.
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