The intestinal microbiota is essential for the host to ensure digestive and immunologic homeostasis. When microbiota homeostasis is impaired and dysbiosis occurs, the malfunction of epithelial barrier leads to intestinal and systemic disorders, chiefly immunologic and metabolic. The role of the intestinal tract is crucial in the metabolism of nutrients, drugs, and hormones, including exogenous and endogenous iodothyronines as well as micronutrients involved in thyroid homeostasis. However, the link between thyroid homeostasis and microbiota composition is not yet completely ascertained. A pathogenetic link with dysbiosis has been described in different autoimmune disorders but not yet fully elucidated in autoimmune thyroid disease which represents the most frequent of them. Anyway, it has been suggested that intestinal dysbiosis may trigger autoimmune thyroiditis. Furthermore, hypo- and hyper-thyroidism, often of autoimmune origin, were respectively associated to small intestinal bacterial overgrowth and to changes in microbiota composition. Whether some steps of this thyroid network may be affected by intestinal microbiota composition is briefly discussed below.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
M. Montalto, F. D’Onofrio, A. Gallo, A. Cazzato, G. Gasbarrini, Intestinal microbiota and its functions. Dig. Liver. Dis. Suppl. 3, 30–34 (2009)
M. Arumugam, J. Raes, E. Pelletier, D. Le Paslier, T. Yamada, D.R. Mende, G.R. Fernandes, J. Tap, T. Bruls, J.M. Batto, M. Bertalan, N. Borruel, F. Casellas, L. Fernandez, L. Gautier, T. Hansen, M. Hattori, T. Hayashi, M. Kleerebezem, K. Kurokawa, M. Leclerc, F. Levenez, C. Manichanh, H.B. Nielsen, T. Nielsen, N. Pons, J. Poulain, J. Qin, T. Sicheritz-Ponten, S. Tims, D. Torrents, E. Ugarte, E.G. Zoetendal, J. Wang, F. Guarner, O. Pedersen, W.M. de Vos, S. Brunak, J. Doré, MetaHIT Consortium, M. Antolín, F. Artiguenave, H.M. Blottiere, M. Almeida, C. Brechot, C. Cara, C. Chervaux, A. Cultrone, C. Delorme, G. Denariaz, R. Dervyn, K.U. Foerstner, C. Friss, M. van de Guchte, E. Guedon, F. Haimet, W. Huber, J. van Hylckama-Vlieg, A. Jamet, C. Juste, G. Kaci, J. Knol, O. Lakhdari, S. Layec, K. Le Roux, E. Maguin, A. Mérieux, R. Melo Minardi, C. M’rini, J. Muller, R. Oozeer, J. Parkhill, P. Renault, M. Rescigno, N. Sanchez, S. Sunagawa, A. Torrejon, K. Turner, G. Vandemeulebrouck, E. Varela, Y. Winogradsky, G. Zeller, J. Weissenbach, S.D. Ehrlich, P. Bork, Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011)
D. Festi, R. Schiumerini, C. Birtolo, L. Marzi, L. Montrone, E. Scaioli, A.R. Di Biase, A. Colecchia, Gut microbiota and its pathophysiology in disease paradigms. Dig. Dis. 29, 518–524 (2011)
F. Shanahan, Translating the microbiota to medicine. Nat. Rev. Gastrenterol. Hepatol. 9, 72–74 (2012)
J.M.M. Natividad, E.F. Verdu, Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol. Res. 69, 42–51 (2013)
A.J. Macpherson, N.L. Harris, Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4, 478–485 (2004)
H. Tlaskalová-Hogenová, R. Stěpánková, H. Kozáková, T. Hudcovic, L. Vannucci, L. Tučková, P. Rossmann, T. Hrnčíř, M. Kverka, Z. Zákostelská, K. Klimešová, J. Přibylová, J. Bártová, D. Sanchez, P. Fundová, D. Borovská, D. Srůtková, Z. Zídek, M. Schwarzer, P. Drastich, D.P. Funda, The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 8, 110–120 (2011)
E.C. Lauritano, A.L. Bilotta, M. Gabrielli, E. Scarpellini, A. Lupascu, A. Laginestra, M. Novi, S. Sottili, M. Serricchio, G. Cammarota, G. Gasbarrini, A. Pontecorvi, A. Gasbarrini, Association between hypothyroidism and small intestinal bacterial overgrowth. J. Clin. Endocrinol. Metab. 92, 4180–4184 (2007)
L. Zhou, X. Li, A. Ahmed, D. Wu, L. Liu, J. Qiu, Y. Yan, M. Jin, Y. Xin, Gut microbe analysis between hyperthyroid and healthy individuals. Curr. Microbiol. 69(5), 675–680 (2014)
A.M. Navarro, V.M. Suen, I.M. Souza, J.E. De Oliveira, J.S. Marchini, Patients with severe bowel malabsorption do not have changes in iodine status. Nutrition 21, 895–900 (2005)
J. Hrdina, A. Banning, A. Kipp, G. Loh, M. Blaut, R. Brigelius-Flohé, The gastrointestinal microbiota affects the selenium status and selenoprotein expression in mice. J. Nutr. Biochem. 20, 638–648 (2009)
M. Michalaki, S. Volonakis, I. Mamali, F. Kalfarentzos, A.G. Vagenakis, K.B. Markou, Dietary iodine absorption is not influenced by malabsorptive bariatric surgery. Obes. Surg. 24, 1921–1925 (2014)
R.L. Vought, F.A. Brown, K.H. Sibinovic, G. McDaniel, Effect of changing intestinal bacterial flora on thyroid function in the rat. Horm. Metab. Res. 4, 43–47 (1972)
T.T. Nguyen, J.J. DiStefano 3rd, L.M. Huang, H. Yamada, H.J. Cahnmann, 5′- and 5-deiodinase activities in adult rat cecum and large bowel contents inhibited by intestinal microflora. Am. J. Physiol. 265, E521–E524 (1993)
L. Sabatino, G. Iervasi, P. Ferrazzi, D. Francesconi, I.J. Chopra, A study of iodothyronine 5′-monodeiodinase activities in normal and pathological tissues in man and their comparison with activities in rat tissues. Life Sci. 68, 191–202 (2000)
S.Y. Wu, W.L. Green, W.S. Huang, M.T. Hays, I.J. Chopra, Alternate pathways of thyroid hormone metabolism. Thyroid 15, 943–958 (2005)
M.P. Hazenberg, W.W. de Herder, T.J. Visser, Hydrolysis of iodothyronine conjugates by intestinal bacteria. FEMS Microbiol. Rev. 4, 9–16 (1988)
M.T. Hays, Thyroid hormone and the gut. Endocr. Res. 14, 203–224 (1988)
J.J. DiStefano 3rd, A. de Luze, T.T. Nguyen, Binding and degradation of 3,5,3′-triiodothyronine and thyroxine by rat intestinal bacteria. Am. J. Physiol. 264, E966–E972 (1993)
T.T. Nguyen, J.J. DiStefano 3rd, H. Yamada, Y.M. Yen, Steady state organ distribution and metabolism of thyroxine and 3,5,3′-triiodothyronine in intestines, liver, kidneys, blood, and residual carcass of the rat in vivo. Endocrinology 133, 2973–2983 (1993)
B. Gereben, A. Zeöld, M. Dentice, D. Salvatore, A.C. Bianco, Activation and inactivation of thyroid hormone by deiodinases: local action with general consequences. Cell Mol. Life Sci. 65(4), 570–590 (2008)
A.M. Faria, A.C. Gomes-Santos, J.L. Gonçalves, T.G. Moreira, S.R. Medeiros, L.P. Dourado, D.C. Cara, Food components and the immune system: from tonic agents to allergens. Front. Immunol. 17, 1–16 (2013)
T.T. Macdonald, G. Monteleone, Immunity, inflammation, and allergy in the gut. Science 307, 1920–1925 (2005)
H.J. Wu, E. Wu, The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3, 4–14 (2012)
K. Mori, Y. Nakagawa, H. Ozaki, Does the gut microbiota trigger Hashimoto’s thyroiditis? Discov. Med. 14, 321–326 (2012)
M. Rotondi, L. Chiovato, S. Romagnani, M. Serio, P. Romagnani, Role of chemokines in endocrine autoimmune diseases. Endocr. Rev. 28(5), 492–520 (2007)
E. Bosi, L. Molteni, M.G. Radaelli, L. Folini, I. Fermo, E. Bazzigaluppi, L. Piemonti, M.R. Pastore, R. Paroni, Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 49, 2824–2827 (2006)
F.C. Sasso, O. Carbonara, R. Torella, A. Mezzogiorno, V. Esposito, L. Demagistris, M. Secondulfo, R. Carratu’, D. Iafusco, M. Cartenì, Ultrastructural changes in enterocytes in subjects with Hashimoto’s thyroiditis. Gut 53, 1878–1880 (2004)
A.P. Weetman, Cellular immune responses in autoimmune thyroid disease. Clin. Endocrinol. 61, 405–413 (2004)
I. Horie, N. Abiru, Y. Nagayama, G. Kuriya, O. Saitoh, T. Ichikawa, Y. Iwakura, K. Eguchi, T helper type 17 immune response plays an indispensable role for development of iodine-induced autoimmune thyroiditis in nonobese diabetic-H2h4 mice. Endocrinology 150, 5135–5142 (2009)
C.L. Burek, M.V. Talor, Environmental triggers of autoimmune thyroiditis. J. Autoimmun. 33, 183–189 (2009)
S. Yu, P.K. Maiti, M. Dyson, R. Jain, H. Braley-Mullen, B cell-deficient NOD.H-2h4 mice have CD4+ CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. J. Exp. Med. 203, 349–358 (2006)
B. Deplancke, Gaskins, H.R: Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr. 73, 1131S–1141S (2001)
D. Pabla, F. Akhlaghi, H. Zia, A comparative pH-dissolution profile study of selected commercial levothyroxine products using inductively coupled plasma mass spectrometry. Eur. J. Pharm. Biopharm. 72, 105–110 (2009)
S. Benvenga, L. Bartolone, S. Squadrito, F. Lo Giudice, F. Trimarchi, Delayed intestinal absorption of levothyroxine. Thyroid 5, 249–253 (1995)
W.E. Visser, E.C. Friesema, T.J. Visser, Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol. Endocrinol. 25, 1–14 (2011)
L.F. de Sousa Moraes, L.M. Grzeskowiak, T.F. de Sales Teixeira, C. Gouveia Peluzio Mdo, Intestinal microbiota and probiotics in celiac disease. Clin. Microbiol. Rev. 27, 482–489 (2014)
C. Virili, G. Bassotti, M.G. Santaguida, R. Iuorio, S.C. Del Duca, V. Mercuri, A. Picarelli, P. Gargiulo, L. Gargano, M. Centanni, Atypical celiac disease as cause of increased need for thyroxine: a systematic study. J. Clin. Endocrinol. Metab. 97, E419–E422 (2012)
M. Cellini, M.G. Santaguida, I. Gatto, C. Virili, S.C. Del Duca, N. Brusca, S. Capriello, L. Gargano, M. Centanni, Systematic appraisal of lactose intolerance as cause of increased need for oral thyroxine. J. Clin. Endocrinol. Metab. 99, E1454–E1458 (2014)
M. Ruchała, E. Szczepanek-Parulska, A. Zybek, The influence of lactose intolerance and other gastro-intestinal tract disorders on L-thyroxine absorption. Endokrynol. Pol. 63, 318–323 (2012)
M. Centanni, Thyroxine treatment: absorption, malabsorption, and novel therapeutic approaches. Endocrine 43, 8–9 (2013)
T. He, K. Venema, M.G. Priebe, G.W. Welling, R.J. Brummer, R.J. Vonk, The role of colonic metabolism in lactose intolerance. Eur. J. Clin. Invest. 38, 541–547 (2008)
M.M. Walker, N.J. Talley, Review article: bacteria and pathogenesis of disease in the upper gastrointestinal tract—beyond the era of Helicobacter pylori. Aliment. Pharmacol. Ther. 39, 767–779 (2014)
M. Centanni, L. Gargano, G. Canettieri, N. Viceconti, A. Franchi, G. Delle Fave, B. Annibale, Thyroxine in goiter, Helicobacter pylori infection, and chronic gastritis. N. Engl. J. Med. 354, 1787–1795 (2006)
This study has been supported by “Sapienza” University of Rome—(University Grants—prot.0006345).
The authors have nothing to disclose.
About this article
Cite this article
Virili, C., Centanni, M. Does microbiota composition affect thyroid homeostasis?. Endocrine 49, 583–587 (2015). https://doi.org/10.1007/s12020-014-0509-2
- Intestinal microbiota
- Thyroxine malabsorption
- Autoimmune thyroiditis