Top

Reviews in Endocrine and Metabolic Disorders

Published in:

Open Access 12-10-2023 | Respiratory Microbiota

The relationship between thyroid and human-associated microbiota: A systematic review of reviews

Authors: Camilla Virili, Ilaria Stramazzo, Maria Flavia Bagaglini, Anna Lucia Carretti, Silvia Capriello, Francesco Romanelli, Pierpaolo Trimboli, Marco Centanni

Published in: Reviews in Endocrine and Metabolic Disorders | Issue 1/2024

Abstract

In recent years, a growing number of studies have examined the relationship between thyroid pathophysiology and intestinal microbiota composition. The reciprocal influence between these two entities has been proven so extensive that some authors coined the term "gut-thyroid axis". However, since some papers reported conflicting results, several aspects of this correlation need to be clarified. This systematic review was conceived to achieve more robust information about: 1)the characteristics of gut microbiota composition in patients with the more common morphological, functional and autoimmune disorders of the thyroid; 2)the influence of gut microbial composition on micronutrients that are essential for the maintenance of thyroid homeostasis; 3)the effect of probiotics, prebiotics and synbiotics, some of the most popular over-the-counter products, on thyroid balance; 4)the opportunity to use specific dietary advice. The literature evaluation was made by three authors independently. A five steps strategy was a priori adopted. After duplicates removal, 1106 records were initially found and 38 reviews were finally included in the analysis. The systematic reviews of reviews found that: 1) some significant variations characterize the gut microbiota composition in patients with thyroid disorders. However, geographical clustering of most of the studies prevents drawing definitive conclusions on this topic; 2) the available knowledge about the effect of probiotics and synbiotics are not strong enough to suggest the routine use of these compounds in patients with thyroid disorders; 3) specific elimination nutrition should not be routine suggested to patients, which, instead have to be checked for possible micronutrients and vitamins deficiency, often owed to gastrointestinal autoimmune comorbidities.

Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14:e1002533. https://doi.org/10.1371/journal.pbio.1002533.CrossRefPubMedPubMedCentral

Gupta N, Yadav VK, Gacem A, et al. Deleterious Effect of Air Pollution on Human Microbial Community and Bacterial Flora: A Short Review. Int J Environ Res Public Health. 2022;19:15494. https://doi.org/10.3390/ijerph192315494.CrossRefPubMedPubMedCentral

Frisan T. Co- and polymicrobial infections in the gut mucosa: The host-microbiota-pathogen perspective. Cell Microbiol. 2021;23:e13279. https://doi.org/10.1111/cmi.13279.CrossRefPubMed

Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol. 2016;14:20–32. https://doi.org/10.1038/nrmicro3552.CrossRefPubMed

Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474(11):1823–36. https://doi.org/10.1042/BCJ20160510.CrossRefPubMed

Eberl G. A new vision of immunity: Homeostasis of the superorganism. Mucosal Immunol. 2010;450–60. https://doi.org/10.1038/mi.2010.20.

Benson AK, Kelly SA, Legge R, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A. 2010;107:18933–8. https://doi.org/10.1073/pnas.1007028107.CrossRefPubMedPubMedCentral

Bäckhed F, Fraser CM, Ringel Y, et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012;12(5):611–22. https://doi.org/10.1016/j.chom.2012.10.012.CrossRefPubMed

Tlaskalová-Hogenová H, Stěpánková R, Kozáková H, et al. 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. 2011;8:110–20. https://doi.org/10.1038/cmi.2010.67.CrossRefPubMedPubMedCentral

10.

Harries DJ. The influence of influence of intestinal bacteria upon the thyroid gland. Br Med J. 1923;1:553. https://doi.org/10.1136/bmj.1.3248.553.CrossRefPubMedPubMedCentral

11.

Aromataris E, Fernandez R, Godfrey CM, et al. Summarizing systematic reviews: methodological development, conduct and reporting of an umbrella review approach. Int J Evid Based Healthc. 2015;13:132–40. https://doi.org/10.1097/XEB.0000000000000055.CrossRefPubMed

12.

Mori K, Nakagawa Y, Ozaki H. Does the gut microbiota trigger Hashimoto’s thyroiditis? Discov Med. 2012;14(78):321–6.PubMed

13.

Kunc M, Gabrych A, Witkowski JM. Microbiome impact on metabolism and function of sex, thyroid, growth and parathyroid hormones. Acta Biochim Pol. 2016;63(2):189–201. https://doi.org/10.18388/abp.2015_1093.CrossRefPubMed

14.

Covelli D, Ludgate M. The thyroid, the eyes and the gut: a possible connection. J Endocrinol Invest. 2017;40(6):567–76. https://doi.org/10.1007/s40618-016-0594-6.CrossRefPubMed

15.

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. https://doi.org/10.1016/j.mce.2017.01.053.CrossRefPubMed

16.

Köhling HL, Plummer SF, Marchesi JR, et al. The microbiota and autoimmunity: their role in thyroid autoimmune diseases. Clin Immunol. 2017;183:63–74. https://doi.org/10.1016/j.clim.2017.07.001.CrossRefPubMed

17.

Virili C, Fallahi P, Antonelli A, et al. Gut microbiota and Hashimoto’s thyroiditis. Rev Endocr Metab Disord. 2018;19(4):293–300. https://doi.org/10.1007/s11154-018-9467-y.CrossRefPubMed

18.

Fröhlich E, Wahl R. Microbiota and thyroid interaction in health and disease. Trends Endocrinol Metab. 2019;30(8):479–90. https://doi.org/10.1016/j.tem.2019.05.008.CrossRefPubMed

19.

Ihnatowicz P, Drywień M, Wątor P, et al. The importance of nutritional factors and dietary management of Hashimoto’s thyroiditis. Ann Agric Environ Med. 2020;27(2):184–93. https://doi.org/10.26444/aaem/112331.CrossRefPubMed

20.

Ejtahed HS, Angoorani P, Soroush AR, et al. Our little friends with big roles: alterations of the gut microbiota in thyroid disorders. Endocr Metab Immune Disord Drug Targets. 2020;20(3):344–50. https://doi.org/10.2174/1871530319666190930110605.CrossRefPubMed

21.

Fenneman AC, Rampanelli E, Yin YS, et al. Gut microbiota and metabolites in the pathogenesis of endocrine disease. Biochem Soc Trans. 2020;48(3):915–31. https://doi.org/10.1042/BST20190686.CrossRefPubMed

22.

Knezevic J, Starchl C, Tmava Berisha A, et al. Thyroid-Gut-Axis: how does the microbiota influence thyroid function? Nutrients. 2020;12(6):1769. https://doi.org/10.3390/nu12061769.CrossRefPubMedPubMedCentral

23.

Masetti G, Ludgate M. Microbiome and Graves’ orbitopathy. Eur Thyroid J. 2020;9(Suppl 1):78–85. https://doi.org/10.1159/000512255.CrossRefPubMedPubMedCentral

24.

Opazo MC, Coronado-Arrázola I, Vallejos OP, et al. The impact of the micronutrient iodine in health and diseases. Crit Rev Food Sci Nutr. 2022;62(6):1466–79. https://doi.org/10.1080/10408398.2020.1843398.CrossRefPubMed

25.

Docimo G, Cangiano A, Romano RM, et al. The human microbiota in endocrinology: implications for pathophysiology, treatment, and prognosis in thyroid diseases. Front Endocrinol (Lausanne). 2020;11: 586529. https://doi.org/10.3389/fendo.2020.586529.CrossRefPubMed

26.

Virili C, Stramazzo I, Centanni M. Gut microbiome and thyroid autoimmunity. Best Pract Res Clin Endocrinol Metab. 2021;35(3): 101506. https://doi.org/10.1016/j.beem.2021.101506.CrossRefPubMed

27.

Qi X, Yun C, Pang Y, et al. The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes. 2021;13(1):1–21. https://doi.org/10.1080/19490976.2021.1894070.CrossRefPubMed

28.

Sturov N, Popov S, Kostenko A, et al. Characteristics of gut microbiota in autoimmune diseases of the thyroid gland and the methods of its correction. Archiv Euromedica. 2021;2(2). https://doi.org/10.35630/2199-885X/2021/11/2/21.

29.

Fernández-García V, González-Ramos S, Martín-Sanz P, et al. Beyond classic concepts in thyroid homeostasis: Immune system and microbiota. Mol Cell Endocrinol. 2021;533: 111333. https://doi.org/10.1016/j.mce.2021.111333.CrossRefPubMed

30.

Ferreira RLU, Sena-Evangelista KCM, de Azevedo EP, et al. Selenium in human health and gut microbiota: bioavailability of selenocompounds and relationship with diseases. Front Nutr. 2021;8: 685317. https://doi.org/10.3389/fnut.2021.685317.CrossRefPubMedPubMedCentral

31.

Bargiel P, Szczuko M, Stachowska L, et al. Microbiome metabolites and thyroid dysfunction. J Clin Med. 2021;10(16):3609. https://doi.org/10.3390/jcm10163609.CrossRefPubMedPubMedCentral

32.

Cao J, Su Y, Chen Z, et al. The risk factors for Graves’ ophthalmopathy. Graefes Arch Clin Exp Ophthalmol. 2022;260(4):1043–54. https://doi.org/10.1007/s00417-021-05456-x.CrossRefPubMed

33.

Gong B, Wang C, Meng F, et al. Association between gut microbiota and autoimmune thyroid disease: a systematic review and meta-analysis. Front Endocrinol (Lausanne). 2021;12: 774362. https://doi.org/10.3389/fendo.2021.774362.CrossRefPubMed

34.

Hou J, Tang Y, Chen Y, et al. The role of the microbiota in Graves’ disease and Graves’ orbitopathy. Front Cell Infect Microbiol. 2021;11:739707. https://doi.org/10.3389/fcimb.2021.739707.CrossRefPubMedPubMedCentral

35.

Bogusławska J, Godlewska M, Gajda E, et al. Cellular and molecular basis of thyroid autoimmunity. Eur Thyroid J. 2022;11(1):e210024. https://doi.org/10.1530/ETJ-21-0024.CrossRefPubMed

36.

Zhou F, Wang X, Wang L, et al. Genetics, epigenetics, cellular immunology, and gut microbiota: emerging links with Graves’ disease. Front Cell Dev Biol. 2022;9: 794912. https://doi.org/10.3389/fcell.2021.794912.CrossRefPubMedPubMedCentral

37.

Wang Y, Ma XM, Wang X, et al. Emerging insights into the role of epigenetics and gut microbiome in the pathogenesis of Graves’ ophthalmopathy. Front Endocrinol (Lausanne). 2022;12: 788535. https://doi.org/10.3389/fendo.2021.788535.CrossRefPubMed

38.

Liu H, Liu H, Liu C, et al. Gut microbiome and the role of metabolites in the study of Graves’ disease. Front Mol Biosci. 2022;9:841223. https://doi.org/10.3389/fmolb.2022.841223.CrossRefPubMedPubMedCentral

39.

Danailova Y, Velikova T, Nikolaev G, et al. Nutritional management of thyroiditis of Hashimoto. Int J Mol Sci. 2022;23(9):5144. https://doi.org/10.3390/ijms23095144.CrossRefPubMedPubMedCentral

40.

Liu Q, Sun W, Zhang H. Interaction of gut microbiota with endocrine homeostasis and thyroid cancer. Cancers (Basel). 2022;14(11):2656. https://doi.org/10.3390/cancers14112656.CrossRefPubMed

41.

Jiang W, Lu G, Gao D, et al. The relationships between the gut microbiota and its metabolites with thyroid diseases. Front Endocrinol (Lausanne). 2022;13: 943408. https://doi.org/10.3389/fendo.2022.943408.CrossRefPubMed

42.

Belvoncikova P, Maronek M, Gardlik R. Gut dysbiosis and fecal microbiota transplantation in autoimmune diseases. Int J Mol Sci. 2022;23(18):10729. https://doi.org/10.3390/ijms231810729.CrossRefPubMedPubMedCentral

43.

Calcaterra V, Mameli C, Rossi V, et al. What we know about the relationship between autoimmune thyroid diseases and gut microbiota: a perspective on the role of probiotics on pediatric endocrinology. Minerva Pediatr (Torino). 2022;74(6):650–71. https://doi.org/10.23736/S2724-5276.22.06873-2.CrossRefPubMed

44.

Sawicka-Gutaj N, Gruszczyński D, Zawalna N, et al. Microbiota alterations in patients with autoimmune thyroid diseases: a systematic review. Int J Mol Sci. 2022;23(21):13450. https://doi.org/10.3390/ijms232113450.CrossRefPubMedPubMedCentral

45.

Wu Z, Tian E, Chen Y, et al. Gut microbiota and its roles in the pathogenesis and therapy of endocrine system diseases. Microbiol Res. 2023;268: 127291. https://doi.org/10.1016/j.micres.2022.127291.CrossRefPubMed

46.

Macvanin MT, Gluvic Z, Zafirovic S, et al. The protective role of nutritional antioxidants against oxidative stress in thyroid disorders. Front Endocrinol (Lausanne). 2023;13:1092837. https://doi.org/10.3389/fendo.2022.1092837.CrossRefPubMed

47.

Fenneman AC, Bruinstroop E, Nieuwdorp M, et al. A comprehensive review of thyroid hormone metabolism in the gut and its clinical implications. Thyroid. 2023;33(1):32–44. https://doi.org/10.1089/thy.2022.0491.Erratum.In:Thyroid.2023Apr;33(4):534.CrossRefPubMed

48.

Stramazzo I, Capriello S, Filardo S, et al. Microbiota and thyroid disease: An updated systematic review. Adv Exp Med Biol. 2023;1370:125–44. https://doi.org/10.1007/5584_2023_770.CrossRefPubMed

49.

Zawadzka K, Kałuzińska K, Świerz MJ, et al. Are probiotics, prebiotics, and synbiotics beneficial in primary thyroid diseases? A systematic review with meta-analysis. Ann Agric Environ Med. 2023;30(2):217–23. https://doi.org/10.26444/aaem/162732.CrossRefPubMed

50.

Lerner A, Jeremias P, Matthias T. Gut-thyroid axis and celiac disease. Endocr Connect. 2017;6:R52–8. https://doi.org/10.1530/EC-17-0021.CrossRefPubMedPubMedCentral

51.

Frau C, Godart M, Plateroti M. Thyroid hormone regulation of intestinal epithelial stem cell biology. Mol Cell Endocrinol. 2017;459:90–7. https://doi.org/10.1016/j.mce.2017.03.002.CrossRefPubMed

52.

Malo MS, Zhang W, Alkhoury F, et al. Thyroid hormone positively regulates the enterocyte differentiation marker intestinal alkaline phosphatase gene via an atypical response element. Mol Endocrinol. 2004;18(8):1941–62. https://doi.org/10.1210/me.2003-0351.CrossRefPubMed

53.

Malo MS, Nasrin Alam S, Mostafa G, et al. Intestinal alkaline phosphatase preserves the normal homeostasis of gut microbiota. Gut. 2010;59(11):1476–84. https://doi.org/10.1136/gut.2010.211706.CrossRefPubMed

54.

Inczefi O, Bacsur P, Resál T, et al. The influence of nutrition on intestinal permeability and the microbiome in health and disease. Front Nutr. 2022;9: 718710. https://doi.org/10.3389/fnut.2022.718710.CrossRefPubMedPubMedCentral

55.

Christovich A, Luo XM. Gut microbiota, leaky gut, and autoimmune diseases. Front Immunol. 2022;13:946248. https://doi.org/10.3389/fimmu.2022.946248.CrossRefPubMedPubMedCentral

56.

Stojanović I, Saksida T, Miljković Đ, et al. Modulation of intestinal ILC3 for the treatment of type 1 diabetes. Front Immunol. 2021;12:653560. https://doi.org/10.3389/fimmu.2021.653560.CrossRefPubMedPubMedCentral

57.

Lauritano EC, Bilotta AL, Gabrielli M, et al. Association between hypothyroidism and small intestinal bacterial overgrowth. J Clin Endocrinol Metab. 2007;92(11):4180–4. https://doi.org/10.1210/jc.2007-0606.CrossRefPubMed

58.

Zhou L, Li X, Ahmed A, et al. Gut microbe analysis between hyperthyroid and healthy individuals. Curr Microbiol. 2014;69(5):675–80. https://doi.org/10.1007/s00284-014-0640-6.CrossRefPubMed

59.

Neuman H, Debelius JW, Knight R, et al. Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev. 2015;39(4):509–21. https://doi.org/10.1093/femsre/fuu010.CrossRefPubMed

60.

Salvatore G, Covelli I, Roche J. The fixation of thyroid hormones by Escherichia coli and its mechanism. Gen Comp Endocrinol. 1963;3:15–25. https://doi.org/10.1016/0016-6480(63)90042-x.CrossRefPubMed

61.

Nicola JP, Vélez ML, Lucero AM, et al. Functional toll-like receptor 4 conferring lipopolysaccharide responsiveness is expressed in thyroid cells. Endocrinology. 2009;150(1):500–8. https://doi.org/10.1210/en.2008-0345.CrossRefPubMed

62.

Penhale WJ, Young PR. The influence of the normal microbial flora on the susceptibility of rats to experimental autoimmune thyroiditis. Clin Exp Immunol. 1988;72(2):288–92.PubMedPubMedCentral

63.

Benvenga S, Guarneri F. Molecular mimicry and autoimmune thyroid disease. Rev Endocr Metab Disord. 2016;17(4):485–98. https://doi.org/10.1007/s11154-016-9363-2.CrossRefPubMed

64.

Burek CL, Talor MV. Environmental triggers of autoimmune thyroiditis. J Autoimmun. 2009;33(3–4):183–9. https://doi.org/10.1016/j.jaut.2009.09.001.CrossRefPubMedPubMedCentral

65.

Sasso FC, Carbonara O, Torella R, et al. Ultrastructural changes in enterocytes in subjects with Hashimoto’s thyroiditis. Gut. 2004;53(12):1878–80. https://doi.org/10.1136/gut.2004.047498.CrossRefPubMedPubMedCentral

66.

Cayres LCF, de Salis LVV, Rodrigues GSP, et al. Detection of alterations in the gut microbiota and intestinal permeability in patients with Hashimoto thyroiditis. Front Immunol. 2021;12: 579140. https://doi.org/10.3389/fimmu.2021.579140.CrossRefPubMedPubMedCentral

67.

Su X, Zhao Y, Li Y, et al. Gut dysbiosis is associated with primary hypothyroidism with interaction on gut-thyroid axis. Clin Sci (Lond). 2020;134(12):1521–35. https://doi.org/10.1042/CS20200475.CrossRefPubMed

68.

Dong T, Zhao F, Yuan K, et al. Association between serum thyroid-stimulating hormone levels and salivary microbiome shifts. Front Cell Infect Microbiol. 2021;11: 603291. https://doi.org/10.3389/fcimb.2021.603291.CrossRefPubMedPubMedCentral

69.

Virili C, Centanni M. Does microbiota composition affect thyroid homeostasis? Endocrine. 2015;49(3):583–7. https://doi.org/10.1007/s12020-014-0509-2.CrossRefPubMed

70.

Visser TJ, Rutgers M, de Herder WW, et al. Hepatic metabolism, biliary clearance and enterohepatic circulation of thyroid hormone. Acta Med Austriaca. 1988;15(Suppl 1):37–9.PubMed

71.

de Herder WW, Hazenberg MP, Pennock-Schröder AM, et al. Rapid and bacteria-dependent in vitro hydrolysis of iodothyronine-conjugates by intestinal contents of humans and rats. Med Biol. 1986;64(1):31–5.PubMed

72.

Wu SY, Green WL, et al. Alternate pathways of thyroid hormone metabolism. Thyroid. 2005;15(8):943–58. https://doi.org/10.1089/thy.2005.15.943.CrossRefPubMed

73.

Yao Z, Zhao M, Gong Y, et al. Relation of gut microbes and L-thyroxine through altered thyroxine metabolism in subclinical hypothyroidism subjects. Front Cell Infect Microbiol. 2020;10:495. https://doi.org/10.3389/fcimb.2020.00495.CrossRefPubMedPubMedCentral

74.

Masetti G, Moshkelgosha S, Köhling HL, et al. INDIGO consortium. Gut microbiota in experimental murine model of Graves’ orbitopathy established in different environments may modulate clinical presentation of disease. Microbiome. 2018;6(1):97. https://doi.org/10.1186/s40168-018-0478-4.CrossRefPubMedPubMedCentral

75.

Moshkelgosha S, Masetti G, Berchner-Pfannschmidt U, et al. Gut microbiome in BALB/c and C57BL/6J mice undergoing experimental thyroid autoimmunity associate with differences in immunological responses and thyroid function. Horm Metab Res. 2018;50(12):932–41. https://doi.org/10.1055/a-0653-3766.CrossRefPubMed

76.

Moshkelgosha S, Verhasselt HL, Masetti G, et al. INDIGO consortium. Modulating gut microbiota in a mouse model of Graves’ orbitopathy and its impact on induced disease. Microbiome. 2021;9(1):45. https://doi.org/10.1186/s40168-020-00952-4.CrossRefPubMedPubMedCentral

77.

Zheng D, Liao H, Chen S, et al. Elevated levels of circulating biomarkers related to leaky gut syndrome and bacterial translocation are associated with Graves’ disease. Front Endocrinol (Lausanne). 2021;12: 796212. https://doi.org/10.3389/fendo.2021.796212.CrossRefPubMed

78.

Beam A, Clinger E, Hao L. Effect of diet and dietary components on the composition of the gut microbiota. Nutrients. 2021;13(8):2795. https://doi.org/10.3390/nu13082795.CrossRefPubMedPubMedCentral

79.

Shi TT, Hua L, Wang H, et al. The potential link between gut microbiota and serum TRAb in Chinese patients with severe and active Graves’ orbitopathy. Int J Endocrinol. 2019;2019:9736968. https://doi.org/10.1155/2019/9736968.CrossRefPubMedPubMedCentral

80.

Larsen JM. The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology. 2017;151(4):363–74. https://doi.org/10.1111/imm.12760.CrossRefPubMedPubMedCentral

81.

Kiseleva EP, Mikhailopulo KI, Sviridov OV, et al. The role of components of Bifidobacterium and Lactobacillus in pathogenesis and serologic diagnosis of autoimmune thyroid diseases. Benef Microbes. 2011;2(2):139–54. https://doi.org/10.3920/BM2010.0011.CrossRefPubMed

82.

Jiang W, Yu X, Kosik RO, et al. Gut microbiota may play a significant role in the pathogenesis of Graves’ disease. Thyroid. 2021;31(5):810–20. https://doi.org/10.1089/thy.2020.0193.CrossRefPubMedPubMedCentral

83.

Chen J, Wang W, Guo Z, et al. Associations between gut microbiota and thyroidal function status in Chinese patients with Graves’ disease. J Endocrinol Invest. 2021;44(9):1913–26. https://doi.org/10.1007/s40618-021-01507-6.CrossRefPubMed

84.

Ishaq HM, Mohammad IS, Shahzad M, et al. Molecular alteration analysis of human gut microbial composition in Graves’ disease patients. Int J Biol Sci. 2018;14(11):1558–70. https://doi.org/10.7150/ijbs.24151.CrossRefPubMedPubMedCentral

85.

Maier L, Pruteanu M, Kuhn M, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature. 2018;555(7698):623–8. https://doi.org/10.1038/nature25979.CrossRefPubMedPubMedCentral

86.

Sun J, Zhao F, Lin B, et al. Gut microbiota participates in antithyroid drug induced liver injury through the lipopolysaccharide related signaling pathway. Front Pharmacol. 2020;11: 598170. https://doi.org/10.3389/fphar.2020.598170.CrossRefPubMedPubMedCentral

87.

Cooper DS. Antithyroid drugs in the management of patients with Graves’ disease: an evidence-based approach to therapeutic controversies. J Clin Endocrinol Metab. 2003;88(8):3474–81. https://doi.org/10.1210/jc.2003-030185.CrossRefPubMed

88.

Yan HX, An WC, Chen F, et al. Intestinal microbiota changes in Graves’ disease: a prospective clinical study. Biosci Rep. 2020;40(9):BSR20191242. https://doi.org/10.1042/BSR20191242.CrossRefPubMedPubMedCentral

89.

Zhang J, Zhang F, Zhao C, et al. Dysbiosis of the gut microbiome is associated with thyroid cancer and thyroid nodules and correlated with clinical index of thyroid function. Endocrine. 2019;64(3):564–74. https://doi.org/10.1007/s12020-018-1831-x.CrossRefPubMed

90.

Li A, Li T, Gao X, et al. Gut microbiome alterations in patients with thyroid nodules. Front Cell Infect Microbiol. 2021;11: 643968. https://doi.org/10.3389/fcimb.2021.643968.CrossRefPubMedPubMedCentral

91.

Yu X, Jiang W, Kosik RO, et al. Gut microbiota changes and its potential relations with thyroid carcinoma. J Adv Res. 2021;35:61–70. https://doi.org/10.1016/j.jare.2021.04.001.CrossRefPubMedPubMedCentral

92.

Liu CJ, Chen SQ, Zhang SY, et al. The comparison of microbial communities in thyroid tissues from thyroid carcinoma patients. J Microbiol. 2021;59(11):988–1001. https://doi.org/10.1007/s12275-021-1271-9.CrossRefPubMed

93.

Gnanasekar A, Castaneda G, Iyangar A, et al. The intratumor microbiome predicts prognosis across gender and subtypes in papillary thyroid carcinoma. Comput Struct Biotechnol J. 2021;19:1986–97. https://doi.org/10.1016/j.csbj.2021.03.032.CrossRefPubMedPubMedCentral

94.

Dai D, Yang Y, Yang Y, et al. Alterations of thyroid microbiota across different thyroid microhabitats in patients with thyroid carcinoma. J Transl Med. 2021;19(1):488. https://doi.org/10.1186/s12967-021-03167-9.CrossRefPubMedPubMedCentral

95.

Samimi H, Haghpanah V. Gut microbiome and radioiodine-refractory papillary thyroid carcinoma pathophysiology. Trends Endocrinol Metab. 2020;31(9):627–30. https://doi.org/10.1016/j.tem.2020.03.005.CrossRefPubMed

96.

Portulano C, Paroder-Belenitsky M, Carrasco N. The Na+/I- symporter (NIS): mechanism and medical impact. Endocr Rev. 2014;35(1):106–49. https://doi.org/10.1210/er.2012-1036.CrossRefPubMed

97.

Vought RL, Brown FA, Sibinovic KH, et al. Effect of changing intestinal bacterial flora on thyroid function in the rat. Horm Metab Res. 1972;4(1):43–7. https://doi.org/10.1055/s-0028-1094095.CrossRefPubMed

98.

Michalaki M, Volonakis S, Mamali I, et al. Dietary iodine absorption is not influenced by malabsorptive bariatric surgery. Obes Surg. 2014;24(11):1921–5. https://doi.org/10.1007/s11695-014-1255-5.CrossRefPubMed

99.

Klebanoff SJ. Iodination of bacteria: A bactericidal mechanism. J Exp Med. 1967;126(6):1063–78. https://doi.org/10.1084/jem.126.6.1063.CrossRefPubMedPubMedCentral

100.

McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev. 1999;12(1):147–79. https://doi.org/10.1128/CMR.12.1.147.Erratum.In:ClinMicrobiolRev2001Jan;14(1):227.CrossRefPubMedPubMedCentral

101.

Chaves Lopez C, Serio A, Rossi C, et al. Effect of diet supplementation with Ascophyllum nodosum on cow milk composition and microbiota. J Dairy Sci. 2016;99(8):6285–97. https://doi.org/10.3168/jds.2015-10837.CrossRefPubMed

102.

Shen H, Han J, Li Y, et al. Different host-specific responses in thyroid function and gut microbiota modulation between diet-induced obese and normal mice given the same dose of iodine. Appl Microbiol Biotechnol. 2019;103(8):3537–47. https://doi.org/10.1007/s00253-019-09687-1.CrossRefPubMed

103.

Duntas LH. The Role of Iodine and Selenium in Autoimmune Thyroiditis. Horm Metab Res. 2015;47(10):721–6. https://doi.org/10.1055/s-0035-1559631.CrossRefPubMed

104.

Hrdina J, Banning A, Kipp A, et al. The gastrointestinal microbiota affects the selenium status and selenoprotein expression in mice. J Nutr Biochem. 2009;20(8):638–48. https://doi.org/10.1016/j.jnutbio.2008.06.009.CrossRefPubMed

105.

Kasaikina MV, Kravtsova MA, Lee BC, et al. Dietary selenium affects host selenoproteome expression by influencing the gut microbiota. FASEB J. 2011;25(7):2492–9. https://doi.org/10.1096/fj.11-181990.CrossRefPubMedPubMedCentral

106.

Zhai Q, Cen S, Li P, et al. Effects of dietary selenium supplementation on intestinal barrier and immune responses associated with its modulation of gut microbiota. Environ Sci Technol Lett. 2018;5:724–30. https://doi.org/10.1021/acs.estlett.8b00563.CrossRef

107.

Marcocci C, Kahaly GJ, Krassas GE, et al. European Group on Graves’ Orbitopathy. Selenium and the course of mild Graves’ orbitopathy. N Engl J Med. 2011;364(20):1920–31. https://doi.org/10.1056/NEJMoa1012985.CrossRefPubMed

108.

Bartalena L, Kahaly GJ, Baldeschi L, et al. EUGOGO †. The 2021 European Group on Graves’ orbitopathy (EUGOGO) clinical practice guidelines for the medical management of Graves’orbitopathy. Eur J Endocrinol. 2021;185(4):G43–67. https://doi.org/10.1530/EJE-21-0479.CrossRefPubMed

109.

Skrypnik K, Suliburska J. Association between the gut microbiota and mineral metabolism. J Sci Food Agric. 2018;98(7):2449–60. https://doi.org/10.1002/jsfa.8724.CrossRefPubMed

110.

Yilmaz B, Li H. Gut microbiota and iron: The crucial actors in health and disease. Pharmaceuticals (Basel). 2018;11(4):98. https://doi.org/10.3390/ph11040098.CrossRefPubMed

111.

Chieppa M, Giannelli G. Immune cells and microbiota response to iron starvation. Front Med (Lausanne). 2018;5:109. https://doi.org/10.3389/fmed.2018.00109.CrossRefPubMed

112.

Beserra JB, Morais JBS, Severo JS, et al. Relation between zinc and thyroid hormones in humans: a systematic review. Biol Trace Elem Res. 2021;199(11):4092–100. https://doi.org/10.1007/s12011-020-02562-5.Erratum.In:BiolTraceElemRes.2021May7.CrossRefPubMed

113.

Usama U, Khan MJ, Fatima S. Role of zinc in shaping the gut microbiome; proposed mechanisms and evidence from the literature. J Gastrointest Dig Syst. 2018;8(1).

114.

Redondo-Useros N, Nova E, González-Zancada N, et al. Microbiota and lifestyle: a special focus on diet. Nutrients. 2020;12:1776. https://doi.org/10.3390/nu12061776.CrossRefPubMedPubMedCentral

115.

Lerner A, Shoenfeld Y, Matthias T. Adverse effects of gluten ingestion and advantages of gluten withdrawal in nonceliac autoimmune disease. Nutr Rev. 2017;75(12):1046–58. https://doi.org/10.1093/nutrit/nux054. PMID: 29202198.CrossRefPubMed

116.

Malandrini S, Trimboli P, Guzzaloni G, et al. What about TSH and anti-thyroid antibodies in patients with autoimmune thyroiditis and celiac disease using a gluten-free diet? A systematic review. Nutrients. 2022;14(8):1681. https://doi.org/10.3390/nu14081681.CrossRefPubMedPubMedCentral

117.

Jivraj A, Hutchinson JM, Ching E, et al. Micronutrient deficiencies are frequent in adult patients with and without celiac disease on a gluten-free diet, regardless of duration and adherence to the diet. Nutrition. 2022;103–104: 111809. https://doi.org/10.1016/j.nut.2022.111809.CrossRefPubMed

118.

Lahner E, Conti L, Cicone F, et al. Thyro-entero-gastric autoimmunity: Pathophysiology and implications for patient management. Best Pract Res Clin Endocrinol Metab. 2020;34(1):101373. https://doi.org/10.1016/j.beem.2019.101373.

119.

Tonstad S, Nathan E, Oda K, et al. Prevalence of hyperthyroidism according to type of vegetarian diet. Public Health Nutr. 2015;18(8):1482–7. https://doi.org/10.1017/S1368980014002183.CrossRefPubMed

120.

Hill C, Guarner F, Reid G, et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–14. https://doi.org/10.1038/nrgastro.2014.66.CrossRefPubMed

121.

Gibson GR, Hutkins R, Sanders ME, et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491–502. https://doi.org/10.1038/nrgastro.2017.75.CrossRefPubMed

122.

Swanson KS, Gibson GR, Hutkins R, et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol. 2020;17(11):687–701. https://doi.org/10.1038/s41575-020-0344-2.CrossRefPubMedPubMedCentral

123.

Suez J, Zmora N, Segal E, Elinav E. The pros, cons, and many unknowns of probiotics. Nat Med. 2019;25(5):716–29. https://doi.org/10.1038/s41591-019-0439-x.CrossRefPubMed

124.

Sajadi Hezaveh Z, Shidfar F. Probiotic and hypothyroidism. In: Yusuf Olsen, Editor. Probiotics and their role in health and disease. Nova Science Publishers, Inc.; 2021. p. 123–170. ISBN: 978-1-53619-965-9.

125.

Spaggiari G, Brigante G, De Vincentis S, et al. Probiotics ingestion does not directly affect thyroid hormonal parameters in hypothyroid patients on levothyroxine treatment. Front Endocrinol (Lausanne). 2017;8:316. https://doi.org/10.3389/fendo.2017.00316.CrossRefPubMed

126.

Talebi S, Karimifar M, Heidari Z, et al. The effect of synbiotic supplementation on anthropometric indices, appetite, and constipation in people with hypothyroidism: A randomized, double-blind, placebo- controlled trial. Phytother Res. 2020;34:2712–20. https://doi.org/10.1002/ptr.6710.CrossRefPubMed

127.

Talebi S, Karimifar M, Heidari Z, et al. The effects of synbiotic supplementation on thyroid function and inflammation in hypothyroid patients: A randomized, double-blind, placebo-controlled trial. Complement Ther Med. 2020;48: 102234. https://doi.org/10.1016/j.ctim.2019.102234.CrossRefPubMed

128.

Talebi S, Karimifar M, Heidari Z, et al. The effects of synbiotic supplementation on fatigue management and mental health status in levothyroxine-treated patients with hypothyroidism: A randomized, double-blind, placebo-controlled clinical trial study. J Isfahan Med Sch. 2016;38:74–84. https://doi.org/10.22122/JIMS.V38I564.12428.CrossRef

129.

Huo D, Cen C, Chang H, et al. Probiotic Bifidobacterium longum supplied with methimazole improved the thyroid function of Graves’ disease patients through the gut-thyroid axis. Commun Biol. 2021;4(1):1046. https://doi.org/10.1038/s42003-021-02587-z.CrossRefPubMedPubMedCentral

130.

Han Z, Cen C, Ou Q, et al. The potential prebiotic berberine combined with methimazole improved the therapeutic effect of graves’ disease patients through regulating the intestinal microbiome. Front Immunol. 2022;12:826067. https://doi.org/10.3389/fimmu.2021.826067.CrossRefPubMedPubMedCentral

131.

Lin B, Zhao F, Liu Y, et al. Randomized clinical trial: probiotics alleviated oral-gut microbiota dysbiosis and thyroid hormone withdrawal-related complications in thyroid cancer patients before radioiodine therapy following thyroidectomy. Front Endocrinol (Lausanne). 2022;13: 834674. https://doi.org/10.3389/fendo.2022.834674.CrossRefPubMed

132.

Khakisahneh S, Zhang XY, Nouri Z, et al. Cecal microbial transplantation attenuates hyperthyroid-induced thermogenesis in Mongolian gerbils. Microb Biotechnol. 2022;15(3):817–31. https://doi.org/10.1111/1751-7915.13793.CrossRefPubMed

133.

Su X, Yin X, Liu Y, et al. Gut dysbiosis contributes to the imbalance of Treg and Th17 Cells in Graves’ disease patients by propionic acid. J Clin Endocrinol Metab. 2020;105(11):dgaa511. https://doi.org/10.1210/clinem/dgaa511.CrossRefPubMed

Title: The relationship between thyroid and human-associated microbiota: A systematic review of reviews
Authors: Camilla Virili
Ilaria Stramazzo
Maria Flavia Bagaglini
Anna Lucia Carretti
Silvia Capriello
Francesco Romanelli
Pierpaolo Trimboli
Marco Centanni
Publication date: 12-10-2023
Publisher: Springer US
Keywords: Respiratory Microbiota
Probiotics
Hashimoto Thyroiditis
Thyroid Cancer
Thyroid Cancer
Thyroid Cancer
Hypothyroidism
Published in: Reviews in Endocrine and Metabolic Disorders / Issue 1/2024
Print ISSN: 1389-9155
Electronic ISSN: 1573-2606
DOI: https://doi.org/10.1007/s11154-023-09839-9

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2024

Update on anaplastic thyroid carcinoma

Application of radiomics and machine learning to thyroid diseases in nuclear medicine: a systematic review

Current practice in intermediate risk differentiated thyroid cancer – a review

Thyroid cancer and insulin resistance

Molecular imaging and related therapeutic options for medullary thyroid carcinoma: state of the art and future opportunities

Thyroid ultrasound and its ancillary techniques

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials