Advertisement

Gut microbiota and Hashimoto’s thyroiditis

  • Camilla Virili
  • Poupak Fallahi
  • Alessandro Antonelli
  • Salvatore Benvenga
  • Marco Centanni
Article

Abstract

About two third of the human microbial commensal community, namely the gut microbiota, is hosted by the gastrointestinal tract which represents the largest interface of the organism to the external environment. This microbial community co-evolved in a symbiotic relationship with the human beings. Growing evidence support the notion that the microbiota plays a significant role in maintaining nutritional, metabolic and immunologic homeostasis in the host. Microbiota, beside the expected role in maintaining gastrointestinal homeostasis also exerts metabolic functions in nutrients digestion and absorption, detoxification and vitamins’ synthesis. Intestinal microbiota is also key in the correct development of the lymphoid system, 70% of which resides at the intestinal level. Available studies, both in murine models and humans, have shown an altered ratio between the different phyla, which characterize a” normal” gut microbiota, in a number of different disorders including obesity, to which a significant part of the studies on intestinal microbiota has been addressed so far. These variations in gut microbiota composition, known as dysbiosis, has been also described in patients bearing intestinal autoimmune diseases as well as type 1 diabetes mellitus, systemic sclerosis and systemic lupus erythematosus. Being Hashimoto’s thyroiditis the most frequent autoimmune disorder worldwide, the analysis of the reciprocal influence with intestinal microbiota gained interest. The whole thyroid peripheral homeostasis may be sensitive to microbiota changes but there is also evidence that the genesis and progression of autoimmune thyroid disorders may be significantly affected from a changing intestinal microbial composition or even from overt dysbiosis. In this brief review, we focused on the main features which characterize the reciprocal influence between microbiota and thyroid autoimmunity described in the most recent literature.

Keywords

Microbiota Dysbiosis Thyroid autoimmunity Hashimoto’s thyroiditis Probiotic 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474:1823–36.CrossRefGoogle Scholar
  2. 2.
    Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol. 2016;14:20–32.CrossRefGoogle Scholar
  3. 3.
    Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14:e1002533.CrossRefGoogle Scholar
  4. 4.
    Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.CrossRefGoogle Scholar
  5. 5.
    Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science. 2016;352:539–44.CrossRefGoogle Scholar
  6. 6.
    Chow J, Lee SM, Shen Y, Khosravi A, Mazmanian SK. Host-bacterial symbiosis in health and disease. Adv Immunol. 2010;107:243–74.CrossRefGoogle Scholar
  7. 7.
    Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837–48.CrossRefGoogle Scholar
  8. 8.
    Kumar M, Babaei P, Ji B, Nielsen J. Human gut microbiota and healthy aging: recent developments and future prospective. Nutr Healthy Aging. 2016;4:3–16.CrossRefGoogle Scholar
  9. 9.
    Sommer F, Anderson JM, Bharti R, Raes J, Rosenstiel P. The resilience of the intestinal microbiota influences health and disease. Nat Rev Microbiol. 2017;15:630–8.CrossRefGoogle Scholar
  10. 10.
    van de Guchte M, Blottière HM, Doré J. Humans as holobionts: implications for prevention and therapy. Microbiome. 2018;6:81.CrossRefGoogle Scholar
  11. 11.
    Natividad JM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res. 2013;69:42–51.CrossRefGoogle Scholar
  12. 12.
    Pickard JM, Zeng MY, Caruso R, Núñez G. Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease. Immunol Rev. 2017;279:70–89.CrossRefGoogle Scholar
  13. 13.
    Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, et al. Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr. 2018;57:1–24.CrossRefGoogle Scholar
  14. 14.
    LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24:160–8.CrossRefGoogle Scholar
  15. 15.
    Suzuki K, Kawamoto S, Maruya M, Fagarasan S. GALT: organization and dynamics leading to IgA synthesis. Adv Immunol. 2010;107:153–85.CrossRefGoogle Scholar
  16. 16.
    Levy M, Kolodziejczyk AA, Thaiss CA, Elinav E. Dysbiosis and the immune system. Nat Rev Immunol. 2017;17:219–32.  https://doi.org/10.1038/nri.2017.7.CrossRefPubMedGoogle Scholar
  17. 17.
    Arora T, Bäckhed F. The gut microbiota and metabolic disease: current understanding and future perspectives. J Intern Med. 2016;280:339–49.CrossRefGoogle Scholar
  18. 18.
    Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong ML, et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J. 2013;13:514–22.CrossRefGoogle Scholar
  19. 19.
    Rothenberg ME, Saito H, Peebles RS Jr. Advances in mechanisms of allergic disease in 2016. J Allergy Clin Immunol. 2017;140:1622–31.CrossRefGoogle Scholar
  20. 20.
    Mcllroy J, Ianiro G, Mukhopadhya I, Hansen R, Hold GL. Review article: the gut microbiome in inflammatory bowel disease-avenues for microbial management. Aliment Pharmacol Ther. 2018;47:26–42.CrossRefGoogle Scholar
  21. 21.
    Brown CT, Davis-Richardson AG, Giongo A, Gano KA, Crabb DB, Mukherjee N, et al. Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PLoS One. 2011;6:e25792.CrossRefGoogle Scholar
  22. 22.
    Uusitalo U, Liu X, Yang J, Aronsson CA, Hummel S, Butterworth M et al; TEDDY Study Group. Association of Early Exposure of Probiotics and Islet Autoimmunity in the TEDDY Study. JAMA Pediatr. 2016;170:20–8.CrossRefGoogle Scholar
  23. 23.
    Pianta A, Arvikar SL, Strle K, Drouin EE, Wang Q, Costello CE, et al. Two rheumatoid arthritis-specific autoantigens correlate microbial immunity with autoimmune responses in joints. J Clin Invest. 2017;127:2946–56.CrossRefGoogle Scholar
  24. 24.
    Montassier E, Berthelot L, Soulillou JP. Are the decrease in circulating anti-α1,3-Gal IgG and the lower content of galactosyl transferase A1 in the microbiota of patients with multiple sclerosis a novel environmental risk factor for the disease? Mol Immunol. 2018;93:162–5.CrossRefGoogle Scholar
  25. 25.
    Hevia A, Milani C, López P, Cuervo A, Arboleya S, Duranti S, et al. Intestinal dysbiosis associated with systemic lupus erythematosus. MBio. 2014;5:e01548–14.CrossRefGoogle Scholar
  26. 26.
    Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol. 2004;4:478–85.CrossRefGoogle Scholar
  27. 27.
    Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122:107–18.CrossRefGoogle Scholar
  28. 28.
    Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–98.CrossRefGoogle Scholar
  29. 29.
    Sefik E, Geva-Zatorsky N, Oh S, Konnikova L, Zemmour D, McGuire AM, et al. MUCOSAL IMMUNOLOGY. Individual intestinal symbionts induce a distinct population of RORγ+ regulatory T cells. Science. 2015;349:993–7.CrossRefGoogle Scholar
  30. 30.
    Hall JA, Bouladoux N, Sun CM, Wohlfert EA, Blank RB, Zhu Q, et al. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity. 2008;29:637–49.CrossRefGoogle Scholar
  31. 31.
    Feng T, Cong Y, Alexander K, Elson C. Regulation of Toll-like receptor 5 gene expression and function on mucosal dendritic cells. PloS One. 2012;7:e35918.CrossRefGoogle Scholar
  32. 32.
    Hapfelmeier S, Lawson MA, Slack E, Kirundi JK, Stoel M, Heikenwalder M, et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science. 2010;328:1705–9.CrossRefGoogle Scholar
  33. 33.
    Yurkovetskiy LA, Pickard JM, Chervonsky AV. Microbiota and autoimmunity: exploring new avenues. Cell Host Microbe. 2015;17:548–52.CrossRefGoogle Scholar
  34. 34.
    Rosser EC, Oleinika K, Tonon S, Doyle R, Bosma A, Carter NA, et al. Regulatory B cells are induced by gut microbiota-driven interleukin-1β and interleukin-6 production. Nat Med. 2014;20:1334–9.CrossRefGoogle Scholar
  35. 35.
    Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature. 2016;535:65–74.CrossRefGoogle Scholar
  36. 36.
    Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3:4–14.CrossRefGoogle Scholar
  37. 37.
    Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27:104–19.CrossRefGoogle Scholar
  38. 38.
    Alenghat T, Artis D. Epigenomic regulation of host-microbiota interactions. Trends Immunol. 2014;35:518–25.CrossRefGoogle Scholar
  39. 39.
    Antonelli A, Ferrari SM, Corrado A, Di Domenicantonio A, Fallahi P. Autoimmune thyroid disorders. Autoimmun Rev. 2015;14:174–80.CrossRefGoogle Scholar
  40. 40.
    Tomer Y. Mechanisms of autoimmune thyroid diseases: from genetics to epigenetics. Annu Rev Pathol. 2014;9:147–56.CrossRefGoogle Scholar
  41. 41.
    Latrofa F, Fiore E, Rago T, Antonangeli L, Montanelli L, Ricci D, et al. Iodine contributes to thyroid autoimmunity in humans by unmasking a cryptic epitope on thyroglobulin. J Clin Endocrinol Metab. 2013;98:E1768–74.CrossRefGoogle Scholar
  42. 42.
    Obołończyk Ł, Siekierska-Hellmann M, Wiśniewski P, Lewczuk A, Berendt-Obołończyk M, Lakomy A, et al. Epidemiology, risk factors and prognosis of Interferon alpha induced thyroid disorders. A prospective clinical study. Postepy Hig Med Dosw (Online). 2017;71:842–9.CrossRefGoogle Scholar
  43. 43.
    Dineen R, Bogdanet D, Thompson D, Thompson CJ, Behan LA, McKay AP, et al. Endocrinopathies and renal outcomes in lithium therapy: impact of lithium toxicity. QJM. 2017;110:821–7.CrossRefGoogle Scholar
  44. 44.
    Winer A, Bodor JN, Borghaei H. Identifying and managing the adverse effects of immune checkpoint blockade. J Thorac Dis. 2018;10:S480–9.CrossRefGoogle Scholar
  45. 45.
    Wang S, Wu Y, Zuo Z, Zhao Y, Wang K. The effect of vitamin D supplementation on thyroid autoantibody levels in the treatment of autoimmune thyroiditis: a systematic review and a meta-analysis. Endocrine. 2018;59:499–505.CrossRefGoogle Scholar
  46. 46.
    Tomer Y. Hepatitis C and interferon induced thyroiditis. J Autoimmun. 2010;34:J322–6.CrossRefGoogle Scholar
  47. 47.
    Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol. 2008;8:737–44.CrossRefGoogle Scholar
  48. 48.
    Feng M, Li H, Chen SF, Li WF, Zhang FB. Polymorphisms in the vitamin D receptor gene and risk of autoimmune thyroid diseases: a meta-analysis. Endocrine. 2013;43:318–26.CrossRefGoogle Scholar
  49. 49.
    Fujii A, Inoue N, Watanabe M, Kawakami C, Hidaka Y, Hayashizaki Y, et al. TSHR gene polymorphisms in the enhancer regions are most strongly associated with the development of graves' disease, especially intractable disease, and of hashimoto's disease. Thyroid. 2017;27:111–9.CrossRefGoogle Scholar
  50. 50.
    Mizuma T, Watanabe M, Inoue N, Arakawa Y, Tomari S, Hidaka Y, et al. Association of the polymorphisms in the gene encoding thyroglobulin with the development and prognosis of autoimmune thyroid disease. Autoimmunity. 2017;50:386–92.CrossRefGoogle Scholar
  51. 51.
    Ting WH, Chien MN, Lo FS, Wang CH, Huang CY, Lin CL, et al. Association of cytotoxic t-lymphocyte-associated protein 4 (CTLA4) gene polymorphisms with autoimmune thyroid disease in children and adults: case-control study. PLoS One. 2016;1:e0154394.CrossRefGoogle Scholar
  52. 52.
    Dultz G, Matheis N, Dittmar M, Röhrig B, Bender K, Kahaly GJ. The protein tyrosine phosphatase non-receptor type 22 C1858T polymorphism is a joint susceptibility locus for immunthyroiditis and autoimmune diabetes. Thyroid. 2009;19:143–8.CrossRefGoogle Scholar
  53. 53.
    Lee HJ, Li CW, Hammerstad SS, Stefan M, Tomer Y. Immunogenetics of autoimmune thyroid diseases: a comprehensive review. J Autoimmun. 2015;64:82–90.CrossRefGoogle Scholar
  54. 54.
    Wang B, Shao X, Song R, Xu D, Zhang JA. The emerging role of epigenetics in autoimmune thyroid diseases. Front Immunol. 2017;8:396.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Shi Y, Wang H, Su Z, Chen J, Xue Y, Wang S, et al. Differentiation imbalance of Th1/Th17 in peripheral blood mononuclear cells might contribute to pathogenesis of Hashimoto's thyroiditis. Scand J Immunol. 2010;72:250–5.CrossRefGoogle Scholar
  56. 56.
    Santaguida MG, Nardo S, Del Duca SC, Lococo E, Virili C, Gargano L, et al. Increased interleukin-4-positive lymphocytes in patients with Hashimoto's thyroiditis and concurrent non-endocrine autoimmune disorders. Clin Exp Immunol. 2011;165:148–54.CrossRefGoogle Scholar
  57. 57.
    Santaguida MG, Gatto I, Mangino G, Virili C, Stramazzo I, Fallahi P, et al. BREG cells in Hashimoto's thyroiditis isolated or associated to further organ-specific autoimmune diseases. Clin Immunol. 2017;184:42–7.CrossRefGoogle Scholar
  58. 58.
    Kristensen B. Regulatory B and T cell responses in patients with autoimmune thyroid disease and healthy controls. Dan Med J. 2016;63 pii: B5177.Google Scholar
  59. 59.
    Meng S, Badrinarain J, Sibley E, Fang R, Hodin R. Thyroid hormone and the d-type cyclins interact in regulating enterocyte gene transcription. J Gastrointest Surg. 2001;5:49–55.CrossRefGoogle Scholar
  60. 60.
    Wegener M, Wedmann B, Langhoff T, Schaffstein J, Adamek R. Effect of hyperthyroidism on the transit of a caloric solid liquid meal through the stomach, the small intestine, and the colon in man. J Clin Endocrinol Metab. 1992;75:745–9.PubMedGoogle Scholar
  61. 61.
    Devdhar M, Ousman YH, Burman KD. Hypothyroidism. Endocrinol Metab Clin North Am. 2007;36:595–615.CrossRefGoogle Scholar
  62. 62.
    Daher R, Yazbeck T, Jaoude JB, Abboud B. Consequences of dysthyroidism on the digestive tract and viscera. World J Gastroenterol. 2009;15:2834–8.CrossRefGoogle Scholar
  63. 63.
    Tönjes A, Karger S, Koch CA, Paschke R, Tannapfel A, Stumvoll M, et al. Impaired enteral levothyroxine absorption in hypothyroidism refractory to oral therapy after thyroid ablation for papillary thyroid cancer: case report and kinetic studies. Thyroid. 2006;16:1047–51.CrossRefGoogle Scholar
  64. 64.
    Lauritano EC, Bilotta AL, Gabrielli M, Scarpellini E, Lupascu A, Laginestra A, et al. Association between hypothyroidism and small intestinal bacterial overgrowth. J Clin Endocrinol Metab. 2007;92:4180–4.CrossRefGoogle Scholar
  65. 65.
    Zhou L, Li X, Ahmed A, Wu D, Liu L, Qiu J, et al. Gut microbe analysis between hyperthyroid and healthy individuals. Curr Microbiol. 2014;69:675–80.CrossRefGoogle Scholar
  66. 66.
    Vought RL, Brown FA, Sibinovic KH, McDaniel EG. Effect of changing intestinal bacterial flora on thyroid function in the rat. Horm Metab Res. 1972;4:43–7.CrossRefGoogle Scholar
  67. 67.
    Neuman H, Debelius JW, Knight R, Koren O. Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev. 2015;39:509–21.CrossRefGoogle Scholar
  68. 68.
    Virili C, Centanni M. Does microbiota composition affect thyroid homeostasis? Endocrine. 2015;49:583–7.CrossRefGoogle Scholar
  69. 69.
    Virili C, Centanni M. "With a little help from my friends" - The role of microbiota in thyroid hormone metabolism and enterohepatic recycling. Mol Cell Endocrinol. 2017;458:39–43.CrossRefGoogle Scholar
  70. 70.
    de Herder WW, Hazenberg MP, Pennock-Schroder AM, Visser TJ. Hydrolysis of iodothyronine conjugates by intestinal bacteria. FEMS Microbiol Lett. 1985;30:347e351.CrossRefGoogle Scholar
  71. 71.
    de Herder WW, Hazenberg MP, Pennock-Schroder AM, Hennemann G, Visser TJ. Hydrolysis of iodothyronine glucuronides by obligately anaerobic bacteria isolated from human faecal flora. FEMS Microbiol Lett. 1986;35:249e253.CrossRefGoogle Scholar
  72. 72.
    Hoefig CS, Wuensch T, Rijntjes E, Lehmphul I, Daniel H, Schweizer U, et al. Biosynthesis of 3-Iodothyronamine From T4 in Murine Intestinal Tissue. Endocrinology. 2015;156:4356–64.CrossRefGoogle Scholar
  73. 73.
    Hoefig CS, Zucchi R, Köhrle J. Thyronamines and derivatives: physiological relevance, pharmacological actions, and future research directions. Thyroid. 2016;26:1656–73.CrossRefGoogle Scholar
  74. 74.
    Tannock GW. A special fondness for lactobacilli. Appl Environ Microbiol. 2004;70:3189–94.CrossRefGoogle Scholar
  75. 75.
    Sohail MU, Ijaz A, Yousaf MS, Ashraf K, Zaneb H, Aleem M, et al. Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity. Poult Sci. 2010;89:1934–8.CrossRefGoogle Scholar
  76. 76.
    Chotinsky D, Mihaylov R. Effect of probiotics and Avotan on the level of thyroid hormones in the blood plasma of broiler chickens. Bulg J Agric Sci. 2013;19:817–21.Google Scholar
  77. 77.
    Varian BJ, Poutahidis T, Levkovich T, Ibrahim YM, Lakritz JR, Chatzigiagkos A, et al. Beneficial bacteria stimulate youthful thyroid gland activity. J Obes Weight Loss Ther. 2014;4:220.Google Scholar
  78. 78.
    Garn H, Bahn S, Baune BT, Binder EB, Bisgaard H, Chatila TA, et al. Current concepts in chronic inflammatory diseases: interactions between microbes, cellular metabolism, and inflammation. J Allergy Clin Immunol. 2016;138:47–56.CrossRefGoogle Scholar
  79. 79.
    Benvenga S, Guarneri F. Molecular mimicry and autoimmune thyroid disease. Rev Endocr Metab Disord. 2016;17:485–98.CrossRefGoogle Scholar
  80. 80.
    Arata N, Ando T, Unger P, Davies TF. By-stander activation in autoimmune thyroiditis: studies on experimental autoimmune thyroiditisin the GFP+ fluorescent mouse. Clin Immunol. 2006;121:108–17.CrossRefGoogle Scholar
  81. 81.
    Thrasyvoulides A, Lymberi P. Evidence for intramolecular B-cell epitope spreading during experimental immunization with an immunogenic thyroglobulin peptide. Clin Exp Immunol. 2003;132:401–7.CrossRefGoogle Scholar
  82. 82.
    de Oliveira GLV, Leite AZ, Higuchi BS, Gonzaga MI, Mariano VS. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology. 2017;152:1–12.CrossRefGoogle Scholar
  83. 83.
    Sasso FC, Carbonara O, Torella R, Mezzogiorno A, Esposito V, Demagistris L, et al. Ultrastructural changes in enterocytes in subjects with Hashimoto's thyroiditis. Gut. 2004;53:1878–80.CrossRefGoogle Scholar
  84. 84.
    Mu Q, Kirby J, Reilly CM, Luo XM. Leaky gut as a danger signal for autoimmune diseases. Front Immunol. 2017;8:598.CrossRefGoogle Scholar
  85. 85.
    Penhale WJ, Young PR. The influence of the normal microbial flora on the susceptibility of rats to experimental autoimmune thyroiditis. Clin Exp Immunol. 1988;7:288–92.Google Scholar
  86. 86.
    Kiseleva EP, Mikhailopulo KI, Sviridov OV, Novik GI, Knirel YA, Szwajcer DE. The role of components of bifidobacterium and lactobacillus in pathogenesis and serologic diagnosis of autoimmune thyroid diseases. Benef Microbes. 2011;2:139–54.CrossRefGoogle Scholar
  87. 87.
    Zhou JS, Gill HS. Immunostimulatory probiotic Lactobacillus rhamnosus HN001 and Bifidobacterium lactis HN019 do not induce pathological inflammation in mouse model of experimental autoimmune thyroiditis. Int J Food Microbiol. 2005;103:97–104.CrossRefGoogle Scholar
  88. 88.
    Ishaq HM, Mohammad IS, Guo H, Shahzad M, Hou YJ, Ma C, et al. Molecular estimation of alteration in intestinal microbial composition in Hashimoto's thyroiditis patients. Biomed Pharmacother. 2017;95:865–74.CrossRefGoogle Scholar
  89. 89.
    Zhao F, Feng J, Li J, Zhao L, Liu Y, Chen H, et al. Alterations of the gut microbiota in Hashimoto's thyroiditis patients. Thyroid. 2018;28:175–86.CrossRefGoogle Scholar
  90. 90.
    Cosorich I, Dalla-Costa G, Sorini C, Ferrarese R, Messina MJ, Dolpady J, et al. High frequency of intestinal TH17 cells correlates with microbiota alterations and disease activity in multiple sclerosis. Sci Adv. 2017;3:e1700492.CrossRefGoogle Scholar
  91. 91.
    Fallahi P, Ferrari SM, Ruffilli I, Elia G, Biricotti M, Vita R, et al. The association of other autoimmune diseases in patients with autoimmune thyroiditis: review of the literature and report of a large series of patients. Autoimmun Rev. 2016;15:1125–8.CrossRefGoogle Scholar
  92. 92.
    Ferrari SM, Elia G, Virili C, Centanni M, Antonelli A, Fallahi P. Systemic lupus erythematosus and thyroid autoimmunity. Front Endocrinol (Lausanne). 2017;8:138.CrossRefGoogle Scholar
  93. 93.
    Ruffilli I, Ragusa F, Benvenga S, Vita R, Antonelli A, Fallahi P, et al. Psoriasis, psoriatic arthritis, and thyroid autoimmunity. Front Endocrinol (Lausanne). 2017;8:139.CrossRefGoogle Scholar
  94. 94.
    Virili C, Bassotti G, Santaguida MG, Iuorio R, Del Duca SC, Mercuri V, et al. Atypical celiac disease as cause of increased need for thyroxine: a systematic study. J Clin Endocrinol Metab. 2012;97:E419–22.CrossRefGoogle Scholar
  95. 95.
    Cellini M, Santaguida MG, Virili C, Capriello S, Brusca N, Gargano L, et al. Hashimoto's thyroiditis and autoimmune gastritis. Front Endocrinol (Lausanne). 2017;8:92.CrossRefGoogle Scholar
  96. 96.
    Melcescu E, Hogan RB 2nd, Brown K, Boyd SA, Abell TL, Koch CA. The various faces of autoimmune endocrinopathies: non-tumoral hypergastrinemia in a patient with lymphocytic colitis and chronic autoimmune gastritis. Exp Mol Pathol. 2012;93:434–40.CrossRefGoogle Scholar
  97. 97.
    Opazo MC, Ortega-Rocha EM, Coronado-Arrázola I, Bonifaz LC, Boudin H, Neunlist M, et al. Intestinal microbiota influences non-intestinal related autoimmune diseases. Front Microbiol. 2018;9:432.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Endocrinology Section, Department of Medico-Surgical Sciences and Biotechnologies“Sapienza” University of RomeLatinaItaly
  2. 2.Endocrinology UnitSanta Maria Goretti HospitalLatinaItaly
  3. 3.Department of Translational Research and New Technologies in Medicine and SurgeryUniversity of PisaPisaItaly
  4. 4.Department of Clinical and Experimental MedicineUniversity of PisaPisaItaly
  5. 5.Interdepartmental Program of Molecular & Clinical Endocrinology, and Women’s Endocrine HealthUniversity Hospital “G. Martino”MessinaItaly
  6. 6.Department of Clinical and Experimental MedicineUniversity of Messina, Policlinico Universitario G. MartinoMessinaItaly

Personalised recommendations