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Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

Our Little Friends with Big Roles: Alterations of the Gut Microbiota in Thyroid Disorders

Author(s): Hanieh-Sadat Ejtahed, Pooneh Angoorani, Ahmad-Reza Soroush, Seyed-Davar Siadat, Nooshin Shirzad, Shirin Hasani-Ranjbar* and Bagher Larijani

Volume 20, Issue 3, 2020

Page: [344 - 350] Pages: 7

DOI: 10.2174/1871530319666190930110605

Price: $65

Abstract

Background: The thyroid gland influences the metabolic processes in our body by producing thyroid hormones, and thyroid disorders can range from a harmless goiter to life-threatening cancer. A growing number of evidence support the link between gut microbiota composition and thyroid homeostasis. Gut dysbiosis can disrupt the normal gut barrier function, leading to immunologic and metabolic disorders.

Objective: The aim of this review was to discuss the main features of gut dysbiosis associated with different thyroid disorders.

Results: Gut microbiota contributes to thyroid hormone synthesis and hydrolysis of thyroid hormones conjugates. It has been shown that microbial metabolites may play a role in autoimmune thyroid diseases via modulating the immune system. Intestinal microbiota can contribute to the thyroid malignancies via controlling DNA damage and apoptosis and influencing inflammatory reactions by the microbiota- derived metabolites. However, the pathogenic role of altered gut microbiota in different thyroid disorders has not yet fully elucidated.

Conclusion: Further research is needed to assess the role of alterations of the gut microbiota in disease onset and development in order to achieve novel strategies for the prevention and treatment of these diseases.

Keywords: Intestinal microbiota, gut dysbiosis, thyroid hormones, autoimmune thyroid diseases, hyperthyroidism, hypothyroidism.

Graphical Abstract
[1]
Ejtahed, H.S.; Hasani-Ranjbar, S.; Larijani, B. Human Microbiome as an Approach to Personalized Medicine. Altern. Ther. Health Med., 2017, 23(6), 8-9.
[PMID: 28987073]
[2]
Ejtahed, H-S.; Soroush, A-R.; Angoorani, P.; Larijani, B.; Hasani-Ranjbar, S. Gut microbiota as a target in the pathogenesis of metabolic disorders: a new approach to novel therapeutic agents. Horm. Metab. Res., 2016, 48(6), 349-358.
[http://dx.doi.org/10.1055/s-0042-107792] [PMID: 27203411]
[3]
Ejtahed, H.S.; Tito, R.Y.; Siadat, S.D.; Hasani-Ranjbar, S.; Hoseini-Tavassol, Z.; Rymenans, L.; Verbeke, K.; Soroush, A.R.; Raes, J.; Larijani, B. Metformin induces weight loss associated with gut microbiota alteration in non-diabetic obese women: a randomized double-blind clinical trial. Eur. J. Endocrinol., 2018, EJE-18-0826.R1.
[PMID: 30540558]
[4]
Ejtahed, H-S.; Angoorani, P.; Hasani-Ranjbar, S.; Siadat, S-D.; Ghasemi, N.; Larijani, B.; Soroush, A.R. Adaptation of human gut microbiota to bariatric surgeries in morbidly obese patients: A systematic review. Microb. Pathog., 2018, 116, 13-21.
[http://dx.doi.org/10.1016/j.micpath.2017.12.074] [PMID: 29306011]
[5]
Tlaskalová-Hogenová, H.; Stěpánková, R.; Kozáková, H.; Hudcovic, T.; Vannucci, L.; Tučková, L.; Rossmann, P.; Hrnčíř, T.; Kverka, M.; Zákostelská, Z.; Klimešová, K.; Přibylová, J.; Bártová, J.; Sanchez, D.; Fundová, P.; Borovská, D.; Srůtková, D.; Zídek, Z.; Schwarzer, M.; Drastich, P.; Funda, D.P. 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(2), 110-120.
[http://dx.doi.org/10.1038/cmi.2010.67] [PMID: 21278760]
[6]
Lauritano, E.C.; Bilotta, A.L.; Gabrielli, M.; Scarpellini, E.; Lupascu, A.; Laginestra, A.; Novi, M.; Sottili, S.; Serricchio, M.; Cammarota, G.; Gasbarrini, G.; Pontecorvi, A.; Gasbarrini, A. Association between hypothyroidism and small intestinal bacterial overgrowth. J. Clin. Endocrinol. Metab., 2007, 92(11), 4180-4184.
[http://dx.doi.org/10.1210/jc.2007-0606] [PMID: 17698907]
[7]
Zhou, L.; Li, X.; Ahmed, A.; Wu, D.; Liu, L.; Qiu, J.; Yan, Y.; Jin, M.; Xin, Y. Gut microbe analysis between hyperthyroid and healthy individuals. Curr. Microbiol., 2014, 69(5), 675-680.
[http://dx.doi.org/10.1007/s00284-014-0640-6] [PMID: 24969306]
[8]
Virili, C.; Centanni, M. Does microbiota composition affect thyroid homeostasis? Endocrine, 2015, 49(3), 583-587.
[http://dx.doi.org/10.1007/s12020-014-0509-2] [PMID: 25516464]
[9]
Tsavkelova, E.A.; Klimova, S.Iu.; Cherdyntseva, T.A.; Netrusov, A.I. [Hormones and hormone-like substances of microorganisms: a review] Prikl. Biokhim. Mikrobiol., 2006, 42(3), 261-268.
[PMID: 16878539]
[10]
Kunc, M.; Gabrych, A.; Witkowski, J.M. Microbiome impact on metabolism and function of sex, thyroid, growth and parathyroid hormones. Acta Biochim. Pol., 2016, 63(2), 189-201.
[PMID: 26505128]
[11]
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.
[http://dx.doi.org/10.1016/j.mce.2017.01.053] [PMID: 28167127]
[12]
Vought, R.L.; Brown, F.A.; Sibinovic, K.H.; McDaniel, E.G. Effect of changing intestinal bacterial flora on thyroid function in the rat. Horm. Metab. Res., 1972, 4(1), 43-47.
[http://dx.doi.org/10.1055/s-0028-1094095] [PMID: 4110893]
[13]
Köhling, H.L.; Plummer, S.F.; Marchesi, J.R.; Davidge, K.S.; Ludgate, M. The microbiota and autoimmunity: Their role in thyroid autoimmune diseases. Clin. Immunol., 2017, 183, 63-74.
[http://dx.doi.org/10.1016/j.clim.2017.07.001] [PMID: 28689782]
[14]
Marshall, J.C. Lipopolysaccharide: an endotoxin or an exogenous hormone? Clin. Infect. Dis., 2005, 41(Supplement_7), S470-S80.
[http://dx.doi.org/10.1086/432000]
[15]
Fekete, C.; Gereben, B.; Doleschall, M.; Harney, J.W.; Dora, J.M.; Bianco, A.C.; Sarkar, S.; Liposits, Z.; Rand, W.; Emerson, C.; Kacskovics, I.; Larsen, P.R.; Lechan, R.M. Lipopolysaccharide induces type 2 iodothyronine deiodinase in the mediobasal hypothalamus: implications for the nonthyroidal illness syndrome. Endocrinology, 2004, 145(4), 1649-1655.
[http://dx.doi.org/10.1210/en.2003-1439] [PMID: 14684601]
[16]
Baur, A.; Bauer, K.; Jarry, H.; Köhrle, J. Effects of proinflammatory cytokines on anterior pituitary 5′-deiodinase type I and type II. J. Endocrinol., 2000, 167(3), 505-515.
[http://dx.doi.org/10.1677/joe.0.1670505] [PMID: 11115778]
[17]
Beigneux, A.P.; Moser, A.H.; Shigenaga, J.K.; Grunfeld, C.; Feingold, K.R. Sick euthyroid syndrome is associated with decreased TR expression and DNA binding in mouse liver. Am. J. Physiol. Endocrinol. Metab., 2003, 284(1), E228-E236.
[http://dx.doi.org/10.1152/ajpendo.00155.2002] [PMID: 12388159]
[18]
Nicola, J.P.; Nazar, M. Mascanfroni, InDo.; Pellizas, C.G.; Masini-Repiso, AMa. NF-κB p65 subunit mediates lipopolysaccharide-induced Na+/I− symporter gene expression by involving functional interaction with the paired domain transcription factor Pax8. Mol. Endocrinol., 2010, 24(9), 1846-1862.
[http://dx.doi.org/10.1210/me.2010-0102] [PMID: 20667985]
[19]
Vélez, M.L.; Costamagna, E.; Kimura, E.T.; Fozzatti, L.; Pellizas, C.G.; Montesinos, M.M.; Lucero, A.M.; Coleoni, A.H.; Santisteban, P.; Masini-Repiso, A.M. Bacterial lipopolysaccharide stimulates the thyrotropin-dependent thyroglobulin gene expression at the transcriptional level by involving the transcription factors thyroid transcription factor-1 and paired box domain transcription factor 8. Endocrinology, 2006, 147(7), 3260-3275.
[http://dx.doi.org/10.1210/en.2005-0789] [PMID: 16627577]
[20]
Bahn Chair, R.S.; Burch, H.B.; Cooper, D.S.; Garber, J.R.; Greenlee, M.C.; Klein, I.; Laurberg, P.; McDougall, I.R.; Montori, V.M.; Rivkees, S.A.; Ross, D.S.; Sosa, J.A.; Stan, M.N. Hyperthyroidism and other causes of thyrotoxicosis: management guidelines of the American Thyroid Association and American Association of Clinical Endocrinologists. Thyroid, 2011, 21(6), 593-646.
[http://dx.doi.org/10.1089/thy.2010.0417] [PMID: 21510801]
[21]
Antonelli, A.; Ferrari, S.M.; Corrado, A.; Di Domenicantonio, A.; Fallahi, P. Autoimmune thyroid disorders. Autoimmun. Rev., 2015, 14(2), 174-180.
[http://dx.doi.org/10.1016/j.autrev.2014.10.016] [PMID: 25461470]
[22]
Weetman, A.P. Immunity, thyroid function and pregnancy: molecular mechanisms. Nat. Rev. Endocrinol., 2010, 6(6), 311-318.
[http://dx.doi.org/10.1038/nrendo.2010.46] [PMID: 20421883]
[23]
Rees Smith, B.; McLachlan, S.M.; Furmaniak, J. Autoantibodies to the thyrotropin receptor. Endocr. Rev., 1988, 9(1), 106-121.
[http://dx.doi.org/10.1210/edrv-9-1-106] [PMID: 3286231]
[24]
Wu, H-J.; Wu, E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes, 2012, 3(1), 4-14.
[http://dx.doi.org/10.4161/gmic.19320] [PMID: 22356853]
[25]
Rotondi, M.; Chiovato, L.; Romagnani, S.; Serio, M.; Romagnani, P. Role of chemokines in endocrine autoimmune diseases. Endocr. Rev., 2007, 28(5), 492-520.
[http://dx.doi.org/10.1210/er.2006-0044] [PMID: 17475924]
[26]
Sasso, F.C.; Carbonara, O.; Torella, R.; Mezzogiorno, A.; Esposito, V.; Demagistris, L.; Secondulfo, M.; Carratu’, R.; Iafusco, D.; Cartenì, M. Ultrastructural changes in enterocytes in subjects with Hashimoto’s thyroiditis. Gut, 2004, 53(12), 1878-1880.
[http://dx.doi.org/10.1136/gut.2004.047498] [PMID: 15542532]
[27]
Furusawa, Y.; Obata, Y.; Fukuda, S.; Endo, T.A.; Nakato, G.; Takahashi, D.; Nakanishi, Y.; Uetake, C.; Kato, K.; Kato, T.; Takahashi, M.; Fukuda, N.N.; Murakami, S.; Miyauchi, E.; Hino, S.; Atarashi, K.; Onawa, S.; Fujimura, Y.; Lockett, T.; Clarke, J.M.; Topping, D.L.; Tomita, M.; Hori, S.; Ohara, O.; Morita, T.; Koseki, H.; Kikuchi, J.; Honda, K.; Hase, K.; Ohno, H. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature, 2013, 504(7480), 446-450.
[http://dx.doi.org/10.1038/nature12721] [PMID: 24226770]
[28]
Davie, J.R. Inhibition of histone deacetylase activity by butyrate. J. Nutr., 2003, 133(7)(Suppl.), 2485S-2493S.
[http://dx.doi.org/10.1093/jn/133.7.2485S] [PMID: 12840228]
[29]
Zapolska-Downar, D.; Naruszewicz, M. Propionate reduces the cytokine-induced VCAM-1 and ICAM-1 expression by inhibiting nuclear factor-kappa B (NF-kappaB) activation. J. Physiol. Pharmacol., 2009, 60(2), 123-131.
[PMID: 19617655]
[30]
Weetman, A.P. Graves’ disease. N. Engl. J. Med., 2000, 343(17), 1236-1248.
[http://dx.doi.org/10.1056/NEJM200010263431707] [PMID: 11071676]
[31]
Hargreaves, C.E.; Grasso, M.; Hampe, C.S.; Stenkova, A.; Atkinson, S.; Joshua, G.W.; Wren, B.W.; Buckle, A.M.; Dunn-Walters, D.; Banga, J.P. Yersinia enterocolitica provides the link between thyroid-stimulating antibodies and their germline counterparts in Graves’ disease. J. Immunol., 2013, 190(11), 5373-5381.
[http://dx.doi.org/10.4049/jimmunol.1203412] [PMID: 23630351]
[32]
Moshkelgosha, S.; Masetti, G.; Berchner-Pfannschmidt, U.; Verhasselt, H.L.; Horstmann, M.; Diaz-Cano, S.; Noble, A.; Edelman, B.; Covelli, D.; Plummer, S.; Marchesi, J.R.; Ludgate, M.; Biscarini, F.; Eckstein, A.; Banga, J.P. 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), 932-941.
[http://dx.doi.org/10.1055/a-0653-3766] [PMID: 30107619]
[33]
Kaakoush, N.O. Insights into the Role of Erysipelotrichaceae in the Human Host. Front. Cell. Infect. Microbiol., 2015, 5, 84.
[http://dx.doi.org/10.3389/fcimb.2015.00084] [PMID: 26636046]
[34]
Kapatral, V.; Anderson, I.; Ivanova, N.; Reznik, G.; Los, T.; Lykidis, A.; Bhattacharyya, A.; Bartman, A.; Gardner, W.; Grechkin, G.; Zhu, L.; Vasieva, O.; Chu, L.; Kogan, Y.; Chaga, O.; Goltsman, E.; Bernal, A.; Larsen, N.; D’Souza, M.; Walunas, T.; Pusch, G.; Haselkorn, R.; Fonstein, M.; Kyrpides, N.; Overbeek, R. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol., 2002, 184(7), 2005-2018.
[http://dx.doi.org/10.1128/JB.184.7.2005-2018.2002] [PMID: 11889109]
[35]
Kostic, A.D.; Gevers, D.; Pedamallu, C.S.; Michaud, M.; Duke, F.; Earl, A.M.; Ojesina, A.I.; Jung, J.; Bass, A.J.; Tabernero, J.; Baselga, J.; Liu, C.; Shivdasani, R.A.; Ogino, S.; Birren, B.W.; Huttenhower, C.; Garrett, W.S.; Meyerson, M. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res., 2012, 22(2), 292-298.
[http://dx.doi.org/10.1101/gr.126573.111] [PMID: 22009990]
[36]
Erny, D.; Hrabě de Angelis, A.L.; Jaitin, D.; Wieghofer, P.; Staszewski, O.; David, E.; Keren-Shaul, H.; Mahlakoiv, T.; Jakobshagen, K.; Buch, T.; Schwierzeck, V.; Utermöhlen, O.; Chun, E.; Garrett, W.S.; McCoy, K.D.; Diefenbach, A.; Staeheli, P.; Stecher, B.; Amit, I.; Prinz, M. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci., 2015, 18(7), 965-977.
[http://dx.doi.org/10.1038/nn.4030] [PMID: 26030851]
[37]
Barrett, E.; Ross, R.P.; O’Toole, P.W.; Fitzgerald, G.F.; Stanton, C. γ-Aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol., 2012, 113(2), 411-417.
[http://dx.doi.org/10.1111/j.1365-2672.2012.05344.x] [PMID: 22612585]
[38]
Collins, S.M.; Bercik, P. The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology, 2009, 136(6), 2003-2014.
[http://dx.doi.org/10.1053/j.gastro.2009.01.075] [PMID: 19457424]
[39]
Bové, K.B.; Watt, T.; Vogel, A.; Hegedüs, L.; Bjoerner, J.B.; Groenvold, M.; Bonnema, S.J.; Rasmussen, Å.K.; Feldt-Rasmussen, U. Anxiety and depression are more prevalent in patients with graves’ disease than in patients with nodular goitre. Eur. Thyroid J., 2014, 3(3), 173-178.
[http://dx.doi.org/10.1159/000365211] [PMID: 25538899]
[40]
Jonklaas, J.; Bianco, A.C.; Bauer, A.J.; Burman, K.D.; Cappola, A.R.; Celi, F.S.; Cooper, D.S.; Kim, B.W.; Peeters, R.P.; Rosenthal, M.S.; Sawka, A.M. Guidelines for the treatment of hypothyroidism: prepared by the american thyroid association task force on thyroid hormone replacement. Thyroid, 2014, 24(12), 1670-1751.
[http://dx.doi.org/10.1089/thy.2014.0028] [PMID: 25266247]
[41]
Tolhurst, G.; Heffron, H.; Lam, Y.S.; Parker, H.E.; Habib, A.M.; Diakogiannaki, E.; Cameron, J.; Grosse, J.; Reimann, F.; Gribble, F.M. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes, 2012, 61(2), 364-371.
[http://dx.doi.org/10.2337/db11-1019] [PMID: 22190648]
[42]
Lin, H.V.; Frassetto, A.; Kowalik, E.J., Jr; Nawrocki, A.R.; Lu, M.M.; Kosinski, J.R.; Hubert, J.A.; Szeto, D.; Yao, X.; Forrest, G.; Marsh, D.J. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One, 2012, 7(4)e35240
[http://dx.doi.org/10.1371/journal.pone.0035240] [PMID: 22506074]
[43]
Ishiwata, H.; Katoh, K.; Chen, C.; Yonezawa, T.; Sasaki, Y.; Obara, Y. Suppressing actions of butyrate on growth hormone (GH) secretion induced by GH-releasing hormone in rat anterior pituitary cells. Gen. Comp. Endocrinol., 2005, 143(3), 222-230.
[http://dx.doi.org/10.1016/j.ygcen.2005.03.015] [PMID: 15927184]
[44]
Stanley, F.; Samuels, H.H. n-Butyrate effects thyroid hormone stimulation of prolactin production and mRNA levels in GH1 cells. J. Biol. Chem., 1984, 259(15), 9768-9775.
[PMID: 6086648]
[45]
Pearce, E.N.; Farwell, A.P.; Braverman, L.E. Thyroiditis. N. Engl. J. Med., 2003, 348(26), 2646-2655.
[http://dx.doi.org/10.1056/NEJMra021194] [PMID: 12826640]
[46]
Tomer, Y. Mechanisms of autoimmune thyroid diseases: from genetics to epigenetics. Annu. Rev. Pathol., 2014, 9, 147-156.
[http://dx.doi.org/10.1146/annurev-pathol-012513-104713] [PMID: 24460189]
[47]
Fish, E.N. The X-files in immunity: sex-based differences predispose immune responses. Nat. Rev. Immunol., 2008, 8(9), 737-744.
[http://dx.doi.org/10.1038/nri2394] [PMID: 18728636]
[48]
Feng, M.; Li, H.; Chen, S-F.; Li, W-F.; Zhang, F-B. Polymorphisms in the vitamin D receptor gene and risk of autoimmune thyroid diseases: a meta-analysis., 2013.
[http://dx.doi.org/10.1007/s12020-012-9812-y]
[49]
Latrofa, F.; Fiore, E.; Rago, T.; Antonangeli, L.; Montanelli, L.; Ricci, D.; Provenzale, M.A.; Scutari, M.; Frigeri, M.; Tonacchera, M.; Vitti, P. Iodine contributes to thyroid autoimmunity in humans by unmasking a cryptic epitope on thyroglobulin. J. Clin. Endocrinol. Metab., 2013, 98(11), E1768-E1774.
[http://dx.doi.org/10.1210/jc.2013-2912] [PMID: 24064687]
[50]
Obołończyk, Ł.; Siekierska-Hellmann, M.; Wiśniewski, P.; Lewczuk, A.; Berendt-Obołończyk, M.; Lakomy, A. Epidemiology, risk factors and prognosis of Interferon alpha induced thyroid disorders. A Prospective Clinical Study. Advances in Hygiene & Experimental Medicine. Postepy Hig. Med. Dosw., 2017, 71.
[51]
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(3), 499-505.
[http://dx.doi.org/10.1007/s12020-018-1532-5] [PMID: 29388046]
[52]
Virili, C.; Fallahi, P.; Antonelli, A.; Benvenga, S.; Centanni, M. Gut microbiota and Hashimoto’s thyroiditis. Rev. Endocr. Metab. Disord., 2018, 19(4), 293-300.
[http://dx.doi.org/10.1007/s11154-018-9467-y] [PMID: 30294759]
[53]
Tomer, Y. Hepatitis C and interferon induced thyroiditis. J. Autoimmun., 2010, 34(3), J322-J326.
[http://dx.doi.org/10.1016/j.jaut.2009.11.008] [PMID: 20022216]
[54]
Kiseleva, E.P.; Mikhailopulo, K.I.; Sviridov, O.V.; Novik, G.I.; Knirel, Y.A.; Szwajcer Dey, E. The role of components of Bifidobacterium and Lactobacillus in pathogenesis and serologic diagnosis of autoimmune thyroid diseases. Benef. Microbes, 2011, 2(2), 139-154.
[http://dx.doi.org/10.3920/BM2010.0011] [PMID: 21831795]
[55]
Zhou, J.S.; Gill, H.S. 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(1), 97-104.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2004.11.031] [PMID: 16084270]
[56]
Ishaq, H.M.; Mohammad, I.S.; Guo, H.; Shahzad, M.; Hou, Y.J.; Ma, C.; Naseem, Z.; Wu, X.; Shi, P.; Xu, J. Molecular estimation of alteration in intestinal microbial composition in Hashimoto’s thyroiditis patients. Biomed. Pharmacother., 2017, 95, 865-874.
[http://dx.doi.org/10.1016/j.biopha.2017.08.101] [PMID: 28903182]
[57]
Zhao, F.; Feng, J.; Li, J.; Zhao, L.; Liu, Y.; Chen, H.; Jin, Y.; Zhu, B.; Wei, Y. Alterations of the Gut Microbiota in Hashimoto’s Thyroiditis Patients. Thyroid, 2018, 28(2), 175-186.
[http://dx.doi.org/10.1089/thy.2017.0395] [PMID: 29320965]
[58]
Spaggiari, G.; Brigante, G.; De Vincentis, S.; Cattini, U.; Roli, L.; De Santis, M.C.; Baraldi, E.; Tagliavini, S.; Varani, M.; Trenti, T.; Rochira, V.; Simoni, M.; Santi, D. Probiotics Ingestion Does Not Directly Affect Thyroid Hormonal Parameters in Hypothyroid Patients on Levothyroxine Treatment. Front. Endocrinol. (Lausanne), 2017, 8, 316.
[http://dx.doi.org/10.3389/fendo.2017.00316] [PMID: 29184537]
[59]
Visser, T.J.; Peeters, R.P. Metabolism of thyroid hormone., 2000.
[60]
Lim, H.; Devesa, S.S.; Sosa, J.A.; Check, D.; Kitahara, C.M. Trends in thyroid cancer incidence and mortality in the United States, 1974-2013. JAMA, 2017, 317(13), 1338-1348.
[http://dx.doi.org/10.1001/jama.2017.2719] [PMID: 28362912]
[61]
Castaño-Rodríguez, N.; Goh, K-L.; Fock, K.M.; Mitchell, H.M.; Kaakoush, N.O. Dysbiosis of the microbiome in gastric carcinogenesis. Sci. Rep., 2017, 7(1), 15957.
[http://dx.doi.org/10.1038/s41598-017-16289-2] [PMID: 29162924]
[62]
Dzutsev, A.; Badger, J.H.; Perez-Chanona, E.; Roy, S.; Salcedo, R.; Smith, C.K.; Trinchieri, G. Microbes and Cancer. Annu. Rev. Immunol., 2017, 35, 199-228.
[http://dx.doi.org/10.1146/annurev-immunol-051116-052133] [PMID: 28142322]
[63]
Arthur, J.C.; Gharaibeh, R.Z.; Mühlbauer, M.; Perez-Chanona, E.; Uronis, J.M.; McCafferty, J.; Fodor, A.A.; Jobin, C. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat. Commun., 2014, 5, 4724.
[http://dx.doi.org/10.1038/ncomms5724] [PMID: 25182170]
[64]
Dalmasso, G.; Cougnoux, A.; Delmas, J.; Darfeuille-Michaud, A.; Bonnet, R. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes, 2014, 5(5), 675-680.
[http://dx.doi.org/10.4161/19490976.2014.969989] [PMID: 25483338]
[65]
Shen, C.T.; Zhang, Y.; Liu, Y.M.; Yin, S.; Zhang, X.Y.; Wei, W.J.; Sun, Z.K.; Song, H.J.; Qiu, Z.L.; Wang, C.R.; Luo, Q.Y. A distinct serum metabolic signature of distant metastatic papillary thyroid carcinoma. Clin. Endocrinol. (Oxf.), 2017, 87(6), 844-852.
[http://dx.doi.org/10.1111/cen.13437] [PMID: 28755525]
[66]
Payne, C.M.; Weber, C.; Crowley-Skillicorn, C.; Dvorak, K.; Bernstein, H.; Bernstein, C.; Holubec, H.; Dvorakova, B.; Garewal, H. Deoxycholate induces mitochondrial oxidative stress and activates NF-kappaB through multiple mechanisms in HCT-116 colon epithelial cells. Carcinogenesis, 2007, 28(1), 215-222.
[http://dx.doi.org/10.1093/carcin/bgl139] [PMID: 16887864]
[67]
Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer, 2015, 136(5), E359-E386.
[http://dx.doi.org/10.1002/ijc.29210] [PMID: 25220842]
[68]
Zhang, J.; Zhang, F.; Zhao, C.; Xu, Q.; Liang, C.; Yang, Y. Dysbiosis of the gut microbiome is associated with thyroid cancer and thyroid nodules and correlated with clinical index of thyroid function. Endocrine, 2018, 1-11.
[PMID: 30584647]
[69]
Benitez, A.J.; Hoffmann, C.; Muir, A.B.; Dods, K.K.; Spergel, J.M.; Bushman, F.D.; Wang, M.L. Inflammation-associated microbiota in pediatric eosinophilic esophagitis. Microbiome, 2015, 3, 23.
[http://dx.doi.org/10.1186/s40168-015-0085-6] [PMID: 26034601]
[70]
Si, J.; Lee, C.; Ko, G. Oral Microbiota: Microbial Biomarkers of Metabolic Syndrome Independent of Host Genetic Factors. Front. Cell. Infect. Microbiol., 2017, 7, 516.
[http://dx.doi.org/10.3389/fcimb.2017.00516] [PMID: 29326886]
[71]
Feng, J.; Zhao, F.; Sun, J.; Lin, B.; Zhao, L.; Liu, Y. Alterations in the gut microbiota and metabolite profiles of thyroid carcinoma patients. Int. J. Cancer, 2018.
[PMID: 30565661]
[72]
Feng, Q.; Liang, S.; Jia, H.; Stadlmayr, A.; Tang, L.; Lan, Z.; Zhang, D.; Xia, H.; Xu, X.; Jie, Z.; Su, L.; Li, X.; Li, X.; Li, J.; Xiao, L.; Huber-Schönauer, U.; Niederseer, D.; Xu, X.; Al-Aama, J.Y.; Yang, H.; Wang, J.; Kristiansen, K.; Arumugam, M.; Tilg, H.; Datz, C.; Wang, J. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat. Commun., 2015, 6, 6528.
[http://dx.doi.org/10.1038/ncomms7528] [PMID: 25758642]
[73]
Gonçalves, P.; Araújo, J.R.; Di Santo, J.P. A cross-talk between microbiota-derived short-chain fatty acids and the host mucosal immune system regulates intestinal homeostasis and inflammatory bowel disease. Inflamm. Bowel Dis., 2018, 24(3), 558-572.
[http://dx.doi.org/10.1093/ibd/izx029] [PMID: 29462379]
[74]
Yano, Y.; Matsui, T.; Uno, H.; Hirai, F.; Futami, K.; Iwashita, A. Risks and clinical features of colorectal cancer complicating Crohn’s disease in Japanese patients. J. Gastroenterol. Hepatol., 2008, 23(11), 1683-1688.
[http://dx.doi.org/10.1111/j.1440-1746.2008.05532.x] [PMID: 18752557]

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