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Thyroid disorders and gastrointestinal and liver dysfunction: A state of the art review

  • Angelos Kyriacou
    Correspondence
    Corresponding author at: Endocrinology and Diabetes, NW1 Ladywell Building, Salford Royal Hospital, Stott Lane, Salford, Greater Manchester, M6 8HD, UK.
    Affiliations
    Endocrinology and Diabetes, Salford Royal NHS Foundation Trust and University Teaching Hospital, Salford, Greater Manchester, UK
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  • John McLaughlin
    Affiliations
    Institute of Inflammation and Repair, Faculty of Medical and Human Sciences, the University of Manchester, Manchester, UK

    Gastroenterology, Salford Royal NHS Foundation Trust and University Teaching Hospital, Salford, Greater Manchester, UK
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  • Akheel A. Syed
    Affiliations
    Endocrinology and Diabetes, Salford Royal NHS Foundation Trust and University Teaching Hospital, Salford, Greater Manchester, UK

    Manchester Medical School, Faculty of Medical and Human Sciences, the University of Manchester, Manchester, UK
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Published:August 07, 2015DOI:https://doi.org/10.1016/j.ejim.2015.07.017

      Highlights

      • The function of the thyroid and the gut are closely intertwined in both health and disease.
      • Thyroid dysfunction commonly causes various gastrointestinal symptoms.
      • Conversely, some gastrointestinal diseases can mimic thyroid disorders (non-thyroidal illness).
      • Thyroid function should be monitored in patients with gastrointestinal diseases and those on interferon therapies.
      • Medullary thyroid carcinoma should be considered in the differential diagnosis of unexplained, chronic diarrhoea.

      Abstract

      Thyroid disorders commonly impact on the gastrointestinal system and may even present with gastrointestinal symptoms in isolation; for example, metastatic medullary thyroid carcinoma typically presents with diarrhoea. Delays in identifying and treating the underlying thyroid dysfunction may lead to unnecessary investigations and treatment, with ongoing morbidity, and can potentially be life-threatening. Similarly, gastrointestinal diseases can impact on thyroid function tests, and an awareness of the concept and management of non-thyroidal illness is necessary to avoid giving unnecessary thyroid therapies that could potentially exacerbate the underlying gastrointestinal disease. Dual thyroid and gastrointestinal pathologies are also common, with presentations occurring concurrently or sequentially, the latter after a variable time lag that can even extend over decades. Such an association aetiologically relates to the autoimmune background of many thyroid disorders (e.g. Graves' disease and Hashimoto's thyroiditis) and gastrointestinal disorders (e.g. coeliac disease and inflammatory bowel disease); such autoimmune conditions can sometimes occur in the context of autoimmune polyglandular syndrome. Emphasis should also be given to the gastrointestinal side effects of some of the medications used for thyroid disease (e.g. anti-thyroid drugs causing hepatotoxicity) and vice versa (e.g. interferon therapy causing autoimmune thyroid dysfunction). In this review, we discuss disorders of the thyroid-gut axis and identify the evidence base behind the management of such disorders.

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      References

        • Vanderpump M.P.J.
        The epidemiology of thyroid disease.
        Br Med Bull. 2011; 99: 39-51https://doi.org/10.1093/bmb/ldr030
        • Yen P.M.
        Physiological and molecular basis of thyroid hormone action.
        Physiol Rev. 2001; 81: 1097-1142
        • Salvatore D.
        • Davies T.
        • Schlumberger M.-J.
        • Hay I.
        • Larsen P.
        Thyroid physiology and diagnostic evaluation of patients with thyroid disorders.
        in: Melmed S. Polonsky K.S. Larsen P.R. Kronemberg H.M. Williams Textb. 12th ed. Endocrinol. Saunders Elsevier, Philadelphia2011
        • Anders H.J.
        Compression syndromes caused by substernal goitres.
        Postgrad Med J. 1998; 74: 327-329https://doi.org/10.1136/pgmj.74.872.327
        • Chiu W.-Y.
        • Yang C.-C.
        • Huang I.-C.
        • Huang T.-S.
        Dysphagia as a manifestation of thyrotoxicosis: report of three cases and literature review.
        Dysphagia. 2004; 19: 120-124
        • Branski D.
        • Levy J.
        • Globus M.
        • Aviad I.
        • Keren A.
        • Chowers I.
        Dysphagia as a primary manifestation of hyperthyroidism.
        J Clin Gastroenterol. 1984; 6: 437-440
        • Hoogendoorn E.H.
        • Cools B.M.
        Hyperthyroidism as a cause of persistent vomiting.
        Neth J Med. 2004; 62: 293-296
        • Sellin J.H.
        • Vassilopoulou-Sellin R
        The gastrointestinal tract and liver in thyrotoxicosis.
        Warn. Ingbar’s Thyroid. 2000: 622-626
        • Verberg M.F.G.
        • Gillott D.J.
        • Al-Fardan N.
        • Grudzinskas J.G.
        Hyperemesis gravidarum, a literature review.
        Hum Reprod Update. 2006; 13: 207-207https://doi.org/10.1093/humupd/dml050
      1. Patil-Sisodia K, Mestman JH. Graves hyperthyroidism and pregnancy: a clinical update. Endocr Pract n.d.;16:118–29. doi:10.4158/EP09233.RA.

        • Daher R.
        • Yazbeck T.
        • Jaoude J.B.
        • Abboud B.
        Consequences of dysthyroidism on the digestive tract and viscera.
        World J Gastroenterol. 2009; 15: 2834-2838
        • Papa A.
        • Cammarota G.
        • Tursi A.
        • Certo M.
        • Montalto M.
        • Capelli G.
        • et al.
        Effects of propylthiouracil on intestinal transit time and symptoms in hyperthyroid patients.
        Hepatogastroenterology. 1997; 44: 426-429
        • Doran G.R.
        Serum enzyme disturbances in thyrotoxicosis and myxoedema.
        J R Soc Med. 1978; 71: 189-194
        • Huang M.J.
        • Li K.L.
        • Wei J.S.
        • Wu S.S.
        • Fan K.D.
        • Liaw Y.F.
        Sequential liver and bone biochemical changes in hyperthyroidism: prospective controlled follow-up study.
        Am J Gastroenterol. 1994; 89: 1071-1076
        • Malik R.
        • Hodgson H.
        The relationship between the thyroid gland and the liver.
        QJM. 2002; 95: 559-569
        • Choudhary A.M.
        • Roberts I.
        Thyroid storm presenting with liver failure.
        J Clin Gastroenterol. 1999; 29: 318-321
      2. Huang MJ, Liaw YF. Clinical associations between thyroid and liver diseases. J Gastroenterol Hepatol 10:344–50.

        • Williams K.V.
        • Nayak S.
        • Becker D.
        • Reyes J.
        • Burmeister L.A.
        Fifty years of experience with propylthiouracil-associated hepatotoxicity: what have we learned?.
        J Clin Endocrinol Metab. 1997; 82: 1727-1733https://doi.org/10.1210/jcem.82.6.4011
        • Yaylali O.
        • Kirac S.
        • Yilmaz M.
        • Akin F.
        • Yuksel D.
        • Demirkan N.
        • et al.
        Does hypothyroidism affect gastrointestinal motility?.
        Gastroenterol Res Pract. 2009; 2009: 529802https://doi.org/10.1155/2009/529802
        • Holdsworth C.D.
        • Besser G.M.
        Influence of gastric emptying-rate and of insulin response on oral glucose tolerance in thyroid disease.
        Lancet. 1968; 2: 700-702
        • Lauritano E.C.
        • Bilotta A.L.
        • Gabrielli M.
        • Scarpellini E.
        • Lupascu A.
        • Laginestra A.
        • et al.
        Association between hypothyroidism and small intestinal bacterial overgrowth.
        J Clin Endocrinol Metab. 2007; 92: 4180-4184https://doi.org/10.1210/jc.2007-0606
        • Bassotti G.
        • Pagliacci M.C.
        • Nicoletti I.
        • Pelli M.A.
        • Morelli A.
        Intestinal pseudoobstruction secondary to hypothyroidism. Importance of small bowel manometry.
        J Clin Gastroenterol. 1992; 14: 56-58
        • Batke M.
        • Cappell M.S.
        Adynamic ileus and acute colonic pseudo-obstruction.
        Med Clin North Am. 2008; 92 ([ix]): 649-670https://doi.org/10.1016/j.mcna.2008.01.002
        • Maser C.
        • Toset A.
        • Roman S.
        Gastrointestinal manifestations of endocrine disease.
        World J Gastroenterol. 2006; 12: 3174-3179
        • Fukunaga K.
        Refractory gastrointestinal bleeding treated with thyroid hormone replacement.
        J Clin Gastroenterol. 2001; 33: 145-147
        • Bacharach T.
        • Evans J.R.
        Enlargement of the colon secondary to hypothyroidism.
        Ann Intern Med. 1957; 47: 121https://doi.org/10.7326/0003-4819-47-1-121
        • Comte B.
        • Vidal H.
        • Laville M.
        • Riou J.P.
        Influence of thyroid hormones on gluconeogenesis from glycerol in rat hepatocytes: a dose-response study.
        Metabolism. 1990; 39: 259-263
        • Liverini G.
        • Iossa S.
        • Barletta A.
        Relationship between resting metabolism and hepatic metabolism: effect of hypothyroidism and 24 hours fasting.
        Horm Res. 1992; 38: 154-159
        • Mansourian A.R.
        A review of literatures on the adverse effects of thyroid abnormalities and liver disorders: an overview on liver dysfunction and hypothyroidism.
        Pak J Biol Sci. 2013; 16: 1641-1652
        • Liangpunsakul S.
        • Chalasani N.
        Is hypothyroidism a risk factor for non-alcoholic steatohepatitis?.
        J Clin Gastroenterol. 2003; 37: 340-343
        • Gardner C.J.
        • Richardson P.
        • Wong C.
        • Polavarapu N.
        • Kemp G.J.
        • Cuthbertson D.J.
        Hypothyroidism in a patient with non-alcoholic fatty liver disease.
        BMJ. 2011; 342: c7199https://doi.org/10.1136/bmj.c7199
        • Hassan M.M.
        • Kaseb A.
        • Li D.
        • Patt Y.Z.
        • Vauthey J.-N.
        • Thomas M.B.
        • et al.
        Association between hypothyroidism and hepatocellular carcinoma: a case-control study in the United States.
        Hepatology. 2009; 49: 1563-1570https://doi.org/10.1002/hep.22793
        • Ji J.-S.
        • Chae H.-S.
        • Cho Y.-S.
        • Kim H.-K.
        • Kim S.-S.
        • Kim C.-W.
        • et al.
        Myxedema ascites: case report and literature review.
        J Korean Med Sci. 2006; 21: 761-764
        • West J.
        • Logan R.F.A.
        • Hill P.G.
        • Lloyd A.
        • Lewis S.
        • Hubbard R.
        • et al.
        Seroprevalence, correlates, and characteristics of undetected coeliac disease in England.
        Gut. 2003; 52: 960-965
        • Sategna-Guidetti C.
        • Bruno M.
        • Mazza E.
        • Carlino A.
        • Predebon S.
        • Tagliabue M.
        • et al.
        Autoimmune thyroid diseases and coeliac disease.
        Eur J Gastroenterol Hepatol. 1998; 10: 927-931
        • Ch’ng C.L.
        • Jones M.K.
        • Kingham J.G.C.
        Celiac disease and autoimmune thyroid disease.
        Clin Med Res. 2007; 5: 184-192https://doi.org/10.3121/cmr.2007.738
        • Cuoco L.
        • Certo M.
        • Jorizzo R.A.
        • De Vitis I.
        • Tursi A.
        • Papa A.
        • et al.
        Prevalence and early diagnosis of coeliac disease in autoimmune thyroid disorders.
        Ital J Gastroenterol Hepatol. 1999; 31: 283-287
        • West J.
        • Logan R.F.A.
        • Smith C.J.
        • Hubbard R.B.
        • Card T.R.
        Malignancy and mortality in people with coeliac disease: population based cohort study.
        BMJ. 2004; 329: 716-719https://doi.org/10.1136/bmj.38169.486701.7C
        • Valentino R.
        • Savastano S.
        • Tommaselli A.P.
        • Dorato M.
        • Scarpitta M.T.
        • Gigante M.
        • et al.
        Prevalence of coeliac disease in patients with thyroid autoimmunity.
        Horm Res. 1999; 51 ([doi:23344]): 124-127
        • Ramadhan A.
        • Tamilia M.
        Treatment-refractory hypothyroidism.
        CMAJ. 2012; 184: 205-209https://doi.org/10.1503/cmaj.110994
        • Reunala T.
        • Collin P.
        Diseases associated with dermatitis herpetiformis.
        Br J Dermatol. 1997; 136: 315-318
        • Ludvigsson J.F.
        • Bai J.C.
        • Biagi F.
        • Card T.R.
        • Ciacci C.
        • Ciclitira P.J.
        • et al.
        Diagnosis and management of adult coeliac disease: guidelines from the British Society of Gastroenterology.
        Gut. 2014; 63: 1210-1228https://doi.org/10.1136/gutjnl-2013-306578
        • Diamanti A.
        • Ferretti F.
        • Guglielmi R.
        • Panetta F.
        • Colistro F.
        • Cappa M.
        • et al.
        Thyroid autoimmunity in children with coeliac disease: a prospective survey.
        Arch Dis Child. 2011; 96: 1038-1041https://doi.org/10.1136/archdischild-2011-300595
        • Elfström P.
        • Montgomery S.M.
        • Kämpe O.
        • Ekbom A.
        • Ludvigsson J.F.
        Risk of thyroid disease in individuals with celiac disease.
        J Clin Endocrinol Metab. 2008; 93: 3915-3921https://doi.org/10.1210/jc.2008-0798
        • Yakut M.
        Thyroid disorders in patients with inflammatory bowel diseases.
        Int J Clin Med. 2011; 02: 89-92https://doi.org/10.4236/ijcm.2011.22018
        • Bernstein C.N.
        • Wajda A.
        • Blanchard J.F.
        The clustering of other chronic inflammatory diseases in inflammatory bowel disease: a population-based study.
        Gastroenterology. 2005; 129: 827-836https://doi.org/10.1053/j.gastro.2005.06.021
        • Carter M.J.
        • Lobo A.J.
        • Travis S.P.L.
        Guidelines for the management of inflammatory bowel disease in adults.
        Gut. 2004; 53: V1-V16https://doi.org/10.1136/gut.2004.043372
        • Lichtenstein G.R.
        • Hanauer S.B.
        • Sandborn W.J.
        Management of Crohn’s disease in adults.
        Am J Gastroenterol. 2009; 104 ([quiz 464, 484]): 465-483https://doi.org/10.1038/ajg.2008.168
        • Modebe O.
        Autoimmune thyroid disease with ulcerative colitis.
        Postgrad Med J. 1986; 62: 475-476
        • Cesarini M.
        • Angelucci E.
        • Rivera M.
        • Pica R.
        • Paoluzi P.
        • Vernia P.
        • et al.
        Thyroid disorders and inflammatory bowel diseases: retrospective evaluation of 909 patients from an Italian Referral Center.
        Inflamm Bowel Dis. 2010; 16: 186-187https://doi.org/10.1002/ibd.20964
        • Valera M.J.M.
        • Smok S.G.
        • Poniachik T.J.
        • Oksenberg R.D.
        • Silva P.G.
        • Ferrario B.M.
        • et al.
        Primary biliary cirrhosis: a thirteen years experience.
        Rev Med Chil. 2006; 134: 469-474https://doi.org/10.4067/S0034-98872006000400010
        • Elta G.H.
        • Sepersky R.A.
        • Goldberg M.J.
        • Connors C.M.
        • Miller K.B.
        • Kaplan M.M.
        Increased incidence of hypothyroidism in primary biliary cirrhosis.
        Dig Dis Sci. 1983; 28: 971-975
        • Silveira M.G.
        • Mendes F.D.
        • Diehl N.N.
        • Enders F.T.
        • Lindor K.D.
        Thyroid dysfunction in primary biliary cirrhosis, primary sclerosing cholangitis and non-alcoholic fatty liver disease.
        Liver Int. 2009; 29: 1094-1100https://doi.org/10.1111/j.1478-3231.2009.02003.x
        • Kebebew E.
        • Ituarte P.H.
        • Siperstein A.E.
        • Duh Q.Y.
        • Clark O.H.
        Medullary thyroid carcinoma: clinical characteristics, treatment, prognostic factors, and a comparison of staging systems.
        Cancer. 2000; 88: 1139-1148
        • Williams E.D.
        Diarrhoea and thyroid carcinoma.
        Proc R Soc Med. 1966; 59: 602-603
        • Steinfeld C.M.
        • Moertel C.G.
        • Woolner L.B.
        Diarrhea and medullary carcinoma of the thyroid.
        Cancer. 1973; 31: 1237-1239https://doi.org/10.1002/1097-0142(197305)31:5<1237::AID-CNCR2820310530>3.0.CO;2-K
        • Schlumberger M.
        • Bastholt L.
        • Dralle H.
        • Jarzab B.
        • Pacini F.
        • Smit J.W.A.
        2012 European thyroid association guidelines for metastatic medullary thyroid cancer.
        Eur Thyroid J. 2012; 1: 5-14https://doi.org/10.1159/000336977
        • Rambaud J.C.
        • Jian R.
        • Flourié B.
        • Hautefeuille M.
        • Salmeron M.
        • Thuillier F.
        • et al.
        Pathophysiological study of diarrhoea in a patient with medullary thyroid carcinoma. Evidence against a secretory mechanism and for the role of shortened colonic transit time.
        Gut. 1988; 29: 537-543
        • Skrabanek P.
        • Cannon D.
        • Dempsey J.
        • Kirrane J.
        • Neligan M.
        • Powell D.
        Substance P in medullary carcinoma of the thyroid.
        Experientia. 1979; 35: 1259-1260
        • Williams E.D.
        • Karim S.M.
        • Sandler M.
        Prostaglandin secretion by medullary carcinoma of the thyroid. A possible cause of the associated idarrhoea.
        Lancet. 1968; 1: 22-23https://doi.org/10.1016/S0140-6736(68)90010-X
        • Ebert E.C.
        The thyroid and the gut.
        J Clin Gastroenterol. 2010; 44: 402-406https://doi.org/10.1097/MCG.0b013e3181d6bc3e
        • Loviselli A.
        • Oppo A.
        • Velluzzi F.
        • Atzeni F.
        • Mastinu G.L.
        • Farci P.
        • et al.
        Independent expression of serological markers of thyroid autoimmunity and hepatitis virus C infection in the general population: results of a community-based study in northwestern Sardinia.
        J Endocrinol Invest. 2014; 22: 660-665https://doi.org/10.1007/BF03343626
        • Mäki M.
        • Kallonen K.
        • Lähdeaho M.-L.
        • Visakorpi J.K.
        Changing pattern of childhood coeliac disease in Finland.
        Acta Paediatr. 1988; 77: 408-412https://doi.org/10.1111/j.1651-2227.1988.tb10668.x
        • Imagawa A.
        • Itoh N.
        • Hanafusa T.
        • Oda Y.
        • Waguri M.
        • Miyagawa J.
        • et al.
        Autoimmune endocrine disease induced by recombinant interferon-alpha therapy for chronic active type C hepatitis.
        J Clin Endocrinol Metab. 1995; 80: 922-926https://doi.org/10.1210/jcem.80.3.7883851
        • Carella C.
        • Mazziotti G.
        • Morisco F.
        • Manganella G.
        • Rotondi M.
        • Tuccillo C.
        • et al.
        Long-term outcome of interferon-alpha-induced thyroid autoimmunity and prognostic influence of thyroid autoantibody pattern at the end of treatment.
        J Clin Endocrinol Metab. 2001; 86: 1925-1929https://doi.org/10.1210/jcem.86.5.7459
        • Preziati D.
        • La Rosa L.
        • Covini G.
        • Marcelli R.
        • Rescalli S.
        • Persani L.
        • et al.
        Autoimmunity and thyroid function in patients with chronic active hepatitis treated with recombinant interferon alpha-2a.
        Eur J Endocrinol. 1995; 132: 587-593
        • Watanabe U.
        • Hashimoto E.
        • Hisamitsu T.
        • Obata H.
        • Hayashi N.
        The risk factor for development of thyroid disease during interferon-alpha therapy for chronic hepatitis C.
        Am J Gastroenterol. 1994; 89: 399-403
        • Marazuela M.
        • García-Buey L.
        • González-Fernández B.
        • García-Monzón C.
        • Arranz A.
        • Borque M.J.
        • et al.
        Thyroid autoimmune disorders in patients with chronic hepatitis C before and during interferon-alpha therapy.
        Clin Endocrinol (Oxf). 1996; 44: 635-642
        • Koh L.K.
        • Greenspan F.S.
        • Yeo P.P.
        Interferon-alpha induced thyroid dysfunction: three clinical presentations and a review of the literature.
        Thyroid. 1997; 7: 891-896
        • Carella C.
        • Mazziotti G.
        • Amato G.
        • Braverman L.E.
        • Roti E.
        Clinical review 169: Interferon-alpha-related thyroid disease: pathophysiological, epidemiological, and clinical aspects.
        J Clin Endocrinol Metab. 2004; 89: 3656-3661https://doi.org/10.1210/jc.2004-0627
        • Matthews D.C.
        • Syed A.A.
        The role of TSH receptor antibodies in the management of Graves’ disease.
        Eur J Intern Med. 2011; 22: 213-216https://doi.org/10.1016/j.ejim.2011.02.006
        • Barbesino G.
        • Tomer Y.
        Clinical utility of TSH receptor antibodies.
        J Clin Endocrinol Metab. 2013; 98: 2247-2255https://doi.org/10.1210/jc.2012-4309
        • Floreani A.
        • Chiaramonte M.
        • Greggio N.A.
        • Fabris P.
        • De Lazzari F.
        • Naccarato R.
        • et al.
        Organ-specific autoimmunity and genetic predisposition in interferon-treated HCV-related chronic hepatitis patients.
        Ital J Gastroenterol Hepatol. 1998; 30: 71-76
        • Oppenheim Y.
        • Ban Y.
        • Tomer Y.
        Interferon induced autoimmune thyroid disease (AITD): a model for human autoimmunity.
        Autoimmun Rev. 2004; 3: 388-393https://doi.org/10.1016/j.autrev.2004.03.003
        • Warner M.H.
        • Beckett G.J.
        Mechanisms behind the non-thyroidal illness syndrome: an update.
        J Endocrinol. 2010; 205: 1-13https://doi.org/10.1677/JOE-09-0412
        • Van den Berghe G.
        Non-thyroidal illness in the ICU: a syndrome with different faces.
        Thyroid. 2014; 24: 1456-1465https://doi.org/10.1089/thy.2014.0201
        • Fliers E.
        • Bianco A.C.
        • Langouche L.
        • Boelen A.
        Thyroid function in critically ill patients.
        Lancet Diab Endocrinol. 2015; https://doi.org/10.1016/S2213-8587(15)00225-9
        • MacCuish A.
        • Razvi S.
        • Syed A.A.
        Effect of weight loss after gastric bypass surgery on thyroid function in euthyroid people with morbid obesity.
        Clin Obes. 2012; 2: 25-28https://doi.org/10.1111/j.1758-8111.2012.00036.x
        • Knudsen N.
        • Laurberg P.
        • Rasmussen L.B.
        • Bulow I.
        • Perrild H.
        • Ovesen L.
        • et al.
        Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population.
        J Clin Endocrinol Metab. 2005; 90: 4019-4024
        • Svare A.
        • Nilsen T.I.
        • Bjoro T.
        • Asvold B.O.
        • Langhammer A.
        Serum TSH related to measures of body mass: longitudinal data from the HUNT Study, Norway.
        Clin Endocrinol. 2011; 74: 769-775https://doi.org/10.1111/j.1365-2265.2011.04009.x
        • Sari R.
        • Balci M.K.
        • Altunbas H.
        • Karayalcin U.
        The effect of body weight and weight loss on thyroid volume and function in obese women.
        Clin Endocrinol. 2003; 59: 258-262https://doi.org/10.1046/j.1365-2265.2003.01836.x
        • Michalaki M.A.
        • Vagenakis A.G.
        • Leonardou A.S.
        • Argentou M.N.
        • Habeos I.G.
        • Makri M.G.
        • et al.
        Thyroid function in humans with morbid obesity.
        Thyroid. 2006; 16: 73-78https://doi.org/10.1089/thy.2006.16.73
        • Papavramidis S.T.
        • Zisiadis A.C.
        • Karamouzis M.N.
        • Kessissoglou II, I.I.
        • Antoniadou H.A.
        • Aidonopoulos A.P.
        Alterations in thyroid hormones and thyrotropin (TSH) in morbidly obese patients before and after vertical gastroplasty.
        Obes Surg. 1995; 5: 298-301https://doi.org/10.1381/096089295765557674
        • Buscemi S.
        • Verga S.
        • Maneri R.
        • Blunda G.
        • Galluzzo A.
        Influences of obesity and weight loss on thyroid hormones. A 3-3.5-year follow-up study on obese subjects with surgical bilio-pancreatic by-pass.
        J Endocrinol Invest. 1997; 20: 276-281
        • Yashkov Y.I.
        • Vinnitsky L.I.
        • Poroykova M.V.
        • Vorobyova N.T.
        Some hormonal changes before and after vertical banded gastroplasty for severe obesity.
        Obes Surg. 2000; 10: 48-53https://doi.org/10.1381/09608920060674111
        • Moulin de Moraes C.M.
        • Mancini M.C.
        • de Melo M.E.
        • Figueiredo D.A.
        • Villares S.M.
        • Rascovski A.
        • et al.
        Prevalence of subclinical hypothyroidism in a morbidly obese population and improvement after weight loss induced by Roux-en-Y gastric bypass.
        Obes Surg. 2005; 15: 1287-1291https://doi.org/10.1381/096089205774512537
        • Chikunguwo S.
        • Brethauer S.
        • Nirujogi V.
        • Pitt T.
        • Udomsawaengsup S.
        • Chand B.
        • et al.
        Influence of obesity and surgical weight loss on thyroid hormone levels.
        Surg Obes Relat Dis. 2007; 3 ([S1550-7289(07)00576-X [pii]]): 631-636https://doi.org/10.1016/j.soard.2007.07.011
        • Agnihothri R.V.
        • Courville A.B.
        • Linderman J.D.
        • Smith S.
        • Brychta R.
        • Remaley A.
        • et al.
        Moderate weight loss is sufficient to affect thyroid hormone homeostasis and inhibit its peripheral conversion.
        Thyroid. 2014; 24: 19-26https://doi.org/10.1089/thy.2013.0055
        • Dall’Asta C.
        • Paganelli M.
        • Morabito A.
        • Vedani P.
        • Barbieri M.
        • Paolisso G.
        • et al.
        Weight loss through gastric banding: effects on TSH and thyroid hormones in obese subjects with normal thyroid function.
        Obesity (Silver Spring). 2010; 18: 854-857
        • Abu-Ghanem Y.
        • Inbar R.
        • Tyomkin V.
        • Kent I.
        • Berkovich L.
        • Ghinea R.
        • et al.
        Effect of sleeve gastrectomy on thyroid hormone levels.
        Obes Surg. 2014; https://doi.org/10.1007/s11695-014-1415-7
        • Lips M.A.
        • Pijl H.
        • van Klinken J.B.
        • de Groot G.H.
        • Janssen I.M.
        • Van Ramshorst B.
        • et al.
        Roux-en-Y gastric bypass and calorie restriction induce comparable time-dependent effects on thyroid hormone function tests in obese female subjects.
        Eur J Endocrinol. 2013; 169: 339-347https://doi.org/10.1530/eje-13-0339
        • Gniuli D.
        • Leccesi L.
        • Guidone C.
        • Iaconelli A.
        • Chiellini C.
        • Manto A.
        • et al.
        Thyroid function and insulin sensitivity before and after bilio-pancreatic diversion.
        Obes Surg. 2010; 20: 61-68https://doi.org/10.1007/s11695-009-0005-6
        • Padwal R.
        • Brocks D.
        • Sharma A.M.
        A systematic review of drug absorption following bariatric surgery and its theoretical implications.
        Obes Rev. 2010; 11: 41-50https://doi.org/10.1111/j.1467-789X.2009.00614.x
        • Rubio I.G.
        • Galrao A.L.
        • Santo M.A.
        • Zanini A.C.
        • Medeiros-Neto G.
        Levothyroxine absorption in morbidly obese patients before and after Roux-En-Y gastric bypass (RYGB) surgery.
        Obes Surg. 2012; 22: 253-258https://doi.org/10.1007/s11695-011-0452-8
        • Gkotsina M.
        • Michalaki M.
        • Mamali I.
        • Markantes G.
        • Sakellaropoulos G.C.
        • Kalfarentzos F.
        • et al.
        Improved levothyroxine pharmacokinetics after bariatric surgery.
        Thyroid. 2013; 23: 414-419https://doi.org/10.1089/thy.2011.0526