Horm Metab Res 2017; 49(10): 723-731
DOI: 10.1055/s-0043-117893
Review
© Georg Thieme Verlag KG Stuttgart · New York

Subclinical Hyperthyroidism and the Cardiovascular Disease

Alessandro P. Delitala
1   Azienda Ospedaliero-Universitaria di Sassari, Sassari, Italy
› Author Affiliations
Further Information

Publication History

received 18 May 2017

accepted 28 July 2017

Publication Date:
15 September 2017 (online)

Abstract

Thyroid hormone excess has complex metabolic effects, particularly on the cardiovascular system. Treatment of these conditions is universally suggested by international guidelines. Subclinical hyperthyroidism, defined by reduced or suppressed TSH levels in the presence of normal free thyroxine and free triiodothyronine values, is common in the general population and progressively increases with aging, being as high as 15.4% in subjects more than 75 years old and more frequent in subjects with nodular goiter. Subclinical hyperthyroidism is often asymptomatic and the diagnosis is incidentally made during screening exams. However, this form of thyroid disorder has gained attention in the last years for its association with cardiovascular disease, in particular with atrial fibrillation. Less clear are the effects of subclinical hyperthyroidism on blood pressure, stroke, or heart failure. The decision to treat subclinical hyperthyroidism is made on the clinical judge, particularly in elderly patients and/or in the presence of comorbidities.

 
  • References

  • 1 Prejbisz A, Warchol-Celinska E, Lenders JW, Januszewicz A. Cardiovascular risk in primary hyperaldosteronism. Horm Metab Res 2015; 47: 973-980
  • 2 Battocchio M, Rebellato A, Grillo A, Dassie F, Maffei P, Bernardi S, Fabris B, Carretta R, Fallo F. Ambulatory arterial stiffness indexes in cushing's syndrome. Horm Metab Res 2017; 49: 214-220
  • 3 Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev 2005; 26: 704-728
  • 4 Mehran L, Amouzegar A, Rahimabad PK, Tohidi M, Tahmasebinejad Z, Azizi F. Thyroid function and metabolic syndrome: A population-based thyroid study. Horm Metab Res 2017; 49: 192-200
  • 5 Delitala AP, Fanciulli G, Pes GM, Maioli M, Delitala G. Thyroid hormones, metabolic syndrome and its components. Endocr Metab Immune Disord Drug Targets 2017; 17: 56-62
  • 6 Danzi S, Klein I. Thyroid hormone and the cardiovascular system. Med Clin North Am 2012; 96: 257-268
  • 7 Osman F, Franklyn JA, Holder RL, Sheppard MC, Gammage MD. Cardiovascular manifestations of hyperthyroidism before and after antithyroid therapy: a matched case-control study. J Am Coll Cardiol 2007; 49: 71-81
  • 8 Kannan L, Kotus-Bart J, Amanullah A. Prevalence of cardiac arrhythmias in hypothyroid and euthyroid patients. Horm Metab Res 2017; 49: 430-433
  • 9 Delitala AP, Orru M, Filigheddu F, Pilia MG, Delitala G, Ganau A, Saba PS, Decandia F, Scuteri A, Marongiu M, Lakatta EG, Strait J, Cucca F. Serum free thyroxine levels are positively associated with arterial stiffness in the SardiNIA study. Clin Endocrinol (Oxf) 2015; 82: 592-597
  • 10 Volzke H, Robinson DM, Schminke U, Ludemann J, Rettig R, Felix SB, Kessler C, John U, Meng W. Thyroid function and carotid wall thickness. J Clin Endocrinol Metab 2004; 89: 2145-2149
  • 11 Wang J, Zheng X, Sun M, Wang Z, Fu Q, Shi Y, Cao M, Zhu Z, Meng C, Mao J, Yang F, Huang X, Xu J, Zhou H, Duan Y, He W, Zhang M, Yang T. Group RS . Low serum free thyroxine concentrations associate with increased arterial stiffness in euthyroid subjects: a population-based cross-sectional study. Endocrine 2015; 50: 465-473
  • 12 Delitala AP, Filigheddu F, Orru M, AlGhatrif M, Steri M, Pilia MG, Scuteri A, Lobina M, Piras MG, Delitala G, Lakatta EG, Schlessinger D, Cucca F. No evidence of association between subclinical thyroid disorders and common carotid intima medial thickness or atherosclerotic plaque. Nutr Metab Cardiovasc Dis 2015; 25: 1104-1110
  • 13 Peixoto de Miranda EJ, Bittencourt MS, Goulart AC, Santos IS, Mill JG, Schmidt MI, Lotufo PA, Bensenor IJ. Lack of Association Between Subclinical Hypothyroidism and Carotid-Femoral Pulse Wave Velocity in a Cross-Sectional Analysis of the ELSA-Brasil. Am J Hypertens 2017; 30: 81-87
  • 14 Pearce EN. Update in lipid alterations in subclinical hypothyroidism. J Clin Endocrinol Metab 2012; 97: 326-333
  • 15 Delitala AP, Fanciulli G, Maioli M, Delitala G. Subclinical hypothyroidism, lipid metabolism and cardiovascular disease. Eur J Intern Med 2017; 38: 17-24
  • 16 Li C, Tan J, Zhang G, Meng Z, Wang R, Li W, Zheng W. Risk factors of hyperthyroidism with hepatic function injury: A 4-year retrospective study. Horm Metab Res 2015; 47: 209-213
  • 17 Delitala AP, Delitala G, Sioni P, Fanciulli G. Thyroid hormone analogs for the treatment of dyslipidemia: past, present, and future. Curr Med Res Opin 2017; 1-9
  • 18 Scuteri A, Morrell CH, Orru M, Strait JB, Tarasov KV, Ferreli LA, Loi F, Pilia MG, Delitala A, Spurgeon H, Najjar SS, AlGhatrif M, Lakatta EG. Longitudinal perspective on the conundrum of central arterial stiffness, blood pressure, and aging. Hypertension 2014; 64: 1219-1227
  • 19 Ross DS, Burch HB, Cooper DS, Greenlee MC, Laurberg P, Maia AL, Rivkees SA, Samuels M, Sosa JA, Stan MN, Walter MA. 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis. Thyroid 2016; 26: 1343-1421
  • 20 Neumann S, Place RF, Krieger CC, Gershengorn MC. Future prospects for the treatment of Graves' hyperthyroidism and eye disease. Horm Metab Res 2015; 47: 789-796
  • 21 Hollowell JG, Staehling NW, Flanders WD, Hannon WH, Gunter EW, Spencer CA, Braverman LE. Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab 2002; 87: 489-499
  • 22 Delitala AP, Pilia MG, Ferreli L, Loi F, Curreli N, Balaci L, Schlessinger D, Cucca F. Prevalence of unknown thyroid disorders in a Sardinian cohort. Eur J Endocrinol 2014; 171: 143-149
  • 23 Volzke H, Ludemann J, Robinson DM, Spieker KW, Schwahn C, Kramer A, John U, Meng W. The prevalence of undiagnosed thyroid disorders in a previously iodine-deficient area. Thyroid 2003; 13: 803-810
  • 24 Lucas A, Julian MT, Canton A, Castell C, Casamitjana R, Martinez-Caceres EM, Granada ML. Undiagnosed thyroid dysfunction, thyroid antibodies, and iodine excretion in a Mediterranean population. Endocrine 2010; 38: 391-396
  • 25 Laurberg P, Pedersen KM, Hreidarsson A, Sigfusson N, Iversen E, Knudsen PR. Iodine intake and the pattern of thyroid disorders: A comparative epidemiological study of thyroid abnormalities in the elderly in Iceland and in Jutland, Denmark. J Clin Endocrinol Metab 1998; 83: 765-769
  • 26 Aghini-Lombardi F, Antonangeli L, Martino E, Vitti P, Maccherini D, Leoli F, Rago T, Grasso L, Valeriano R, Balestrieri A, Pinchera A. The spectrum of thyroid disorders in an iodine-deficient community: the Pescopagano survey. J Clin Endocrinol Metab 1999; 84: 561-566
  • 27 Knudsen N, Bulow I, Laurberg P, Ovesen L, Perrild H, Jorgensen T. Low socio-economic status and familial occurrence of goitre are associated with a high prevalence of goitre. Eur J Epidemiol 2003; 18: 175-181
  • 28 O'Leary PC, Feddema PH, Michelangeli VP, Leedman PJ, Chew GT, Knuiman M, Kaye J, Walsh JP. Investigations of thyroid hormones and antibodies based on a community health survey: The Busselton thyroid study. Clin Endocrinol (Oxf) 2006; 64: 97-104
  • 29 Tonacchera M, Pinchera A, Vitti P. Assessment of nodular goitre. Best Pract Res Clin Endocrinol Metab 2010; 24: 51-61
  • 30 Vadiveloo T, Donnan PT, Cochrane L, Leese GP. The Thyroid Epidemiology, Audit, and Research Study (TEARS): The natural history of endogenous subclinical hyperthyroidism. J Clin Endocrinol Metab 2011; 96: E1-E8
  • 31 Das G, Ojewuyi TA, Baglioni P, Geen J, Premawardhana LD, Okosieme OE. Serum thyrotrophin at baseline predicts the natural course of subclinical hyperthyroidism. Clin Endocrinol (Oxf) 2012; 77: 146-151
  • 32 Rosario PW. Natural history of subclinical hyperthyroidism in elderly patients with TSH between 0.1 and 0.4 mIU/l: A prospective study. Clin Endocrinol (Oxf) 2010; 72: 685-688
  • 33 Meyerovitch J, Rotman-Pikielny P, Sherf M, Battat E, Levy Y, Surks MI. Serum thyrotropin measurements in the community: Five-year follow-up in a large network of primary care physicians. Arch Intern Med 2007; 167: 1533-1538
  • 34 Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 2002; 23: 38-89
  • 35 Polikar R, Burger AG, Scherrer U, Nicod P. The thyroid and the heart. Circulation 1993; 87: 1435-1441
  • 36 Klein I, Ojamaa K. Thyroid hormone and the cardiovascular system. N Engl J Med 2001; 344: 501-509
  • 37 Baxter JD, Webb P. Thyroid hormone mimetics: Potential applications in atherosclerosis, obesity and type 2 diabetes. Nat Rev Drug Discov 2009; 8: 308-320
  • 38 Weinberger C, Thompson CC, Ong ES, Lebo R, Gruol DJ, Evans RM. The c-erb-A gene encodes a thyroid hormone receptor. Nature 1986; 324: 641-646
  • 39 Apriletti JW, Ribeiro RC, Wagner RL, Feng W, Webb P, Kushner PJ, West BL, Nilsson S, Scanlan TS, Fletterick RJ, Baxter JD. Molecular and structural biology of thyroid hormone receptors. Clin Exp Pharmacol Physiol Suppl 1998; 25: S2-S11
  • 40 Zhu X, Cheng SY. New insights into regulation of lipid metabolism by thyroid hormone. Curr Opin Endocrinol Diabetes Obes 2010; 17: 408-413
  • 41 Kahaly GJ. Cardiovascular and atherogenic aspects of subclinical hypothyroidism. Thyroid 2000; 10: 665-679
  • 42 Schmidt BM, Martin N, Georgens AC, Tillmann HC, Feuring M, Christ M, Wehling M. Nongenomic cardiovascular effects of triiodothyronine in euthyroid male volunteers. J Clin Endocrinol Metab 2002; 87: 1681-1686
  • 43 Sandler G, Wilson GM. The nature and prognosis of heart disease in thyrotoxicosis. A review of 150 patients treated with 131 I. Q J Med 1959; 28: 347-369
  • 44 Nordyke RA, Gilbert Jr FI, Harada AS. Graves’ disease. Influence of age on clinical findings. Arch Intern Med 1988; 148: 626-631
  • 45 Siebers MJ, Drinka PJ, Vergauwen C. Hyperthyroidism as a cause of atrial fibrillation in long-term care. Arch Intern Med 1992; 152: 2063-2064
  • 46 Kirchhof P, Benussi S, Kotecha D, Ahlsson A, Atar D, Casadei B, Castella M, Diener HC, Heidbuchel H, Hendriks J, Hindricks G, Manolis AS, Oldgren J, Popescu BA, Schotten U, Van Putte B, Vardas P, Agewall S, Camm J, Baron Esquivias G, Budts W, Carerj S, Casselman F, Coca A, De Caterina R, Deftereos S, Dobrev D, Ferro JM, Filippatos G, Fitzsimons D, Gorenek B, Guenoun M, Hohnloser SH, Kolh P, Lip GY, Manolis A, McMurray J, Ponikowski P, Rosenhek R, Ruschitzka F, Savelieva I, Sharma S, Suwalski P, Tamargo JL, Taylor CJ, Van Gelder IC, Voors AA, Windecker S, Zamorano JL, Zeppenfeld K. 2016 ESC Guidelines for the management of atrial fibrillation developed in collaboration with EACTS. Eur Heart J 2016; 37: 2893-2962
  • 47 Sawin CT, Geller A, Wolf PA, Belanger AJ, Baker E, Bacharach P, Wilson PW, Benjamin EJ, D'Agostino RB. Low serum thyrotropin concentrations as a risk factor for atrial fibrillation in older persons. N Engl J Med 1994; 331: 1249-1252
  • 48 Auer J, Scheibner P, Mische T, Langsteger W, Eber O, Eber B. Subclinical hyperthyroidism as a risk factor for atrial fibrillation. Am Heart J 2001; 142: 838-842
  • 49 Gammage MD, Parle JV, Holder RL, Roberts LM, Hobbs FD, Wilson S, Sheppard MC, Franklyn JA. Association between serum free thyroxine concentration and atrial fibrillation. Arch Intern Med 2007; 167: 928-934
  • 50 Heeringa J, Hoogendoorn EH, van der Deure WM, Hofman A, Peeters RP, Hop WC, den Heijer M, Visser TJ, Witteman JC. High-normal thyroid function and risk of atrial fibrillation: The Rotterdam study. Arch Intern Med 2008; 168: 2219-2224
  • 51 Vadiveloo T, Donnan PT, Cochrane L, Leese GP. The Thyroid Epidemiology, Audit, and Research Study (TEARS): Morbidity in patients with endogenous subclinical hyperthyroidism. J Clin Endocrinol Metab 2011; 96: 1344-1351
  • 52 Sgarbi JA, Villaca FG, Garbeline B, Villar HE, Romaldini JH. The effects of early antithyroid therapy for endogenous subclinical hyperthyroidism in clinical and heart abnormalities. J Clin Endocrinol Metab 2003; 88: 1672-1677
  • 53 Biondi B, Fazio S, Palmieri EA, Tremalaterra R, Angellotti G, Bone F, Riccio G, Cittadini A, Lombardi G, Sacca L. Effects of chronic subclinical hyperthyroidism from levothyroxine on cardiac morphology and function. Cardiologia 1999; 44: 443-449
  • 54 Gen R, Akbay E, Camsari A, Ozcan T. P-wave dispersion in endogenous and exogenous subclinical hyperthyroidism. J Endocrinol Invest 2010; 33: 88-91
  • 55 Cetinarslan B, Akkoyun M, Canturk Z, Tarkun I, Kahranman G, Komsuoglu B. Duration of the P wave and P wave dispersion in subclinical hyperthyroidism. Endocr Pract 2003; 9: 200-203
  • 56 Aras D, Maden O, Ozdemir O, Aras S, Topaloglu S, Yetkin E, Demir AD, Soylu MO, Erdogan MF, Kisacik HL, Korkmaz S. Simple electrocardiographic markers for the prediction of paroxysmal atrial fibrillation in hyperthyroidism. Int J Cardiol 2005; 99: 59-64
  • 57 Mittelmeier H, Heisel J. Sixteen-years' experience with ceramic hip prostheses. Clin Orthop Relat Res 1992; 64-72
  • 58 Biondi B, Fazio S, Carella C, Amato G, Cittadini A, Lupoli G, Sacca L, Bellastella A, Lombardi G. Cardiac effects of long term thyrotropin-suppressive therapy with levothyroxine. J Clin Endocrinol Metab 1993; 77: 334-338
  • 59 Rosario PW, Carvalho M, Calsolari MR. Symptoms of thyrotoxicosis, bone metabolism and occult atrial fibrillation in older women with mild endogenous subclinical hyperthyroidism. Clin Endocrinol (Oxf) 2016; 85: 132-136
  • 60 Freedberg AS, Papp JG, Williams EM. The effect of altered thyroid state on atrial intracellular potentials. J Physiol 1970; 207: 357-369
  • 61 Mancia G, Fagard R, Narkiewicz K, Redon J, Zanchetti A, Bohm M, Christiaens T, Cifkova R, De Backer G, Dominiczak A, Galderisi M, Grobbee DE, Jaarsma T, Kirchhof P, Kjeldsen SE, Laurent S, Manolis AJ, Nilsson PM, Ruilope LM, Schmieder RE, Sirnes PA, Sleight P, Viigimaa M, Waeber B, Zannad F, Redon J, Dominiczak A, Narkiewicz K, Nilsson PM, Burnier M, Viigimaa M, Ambrosioni E, Caufield M, Coca A, Olsen MH, Schmieder RE, Tsioufis C, van de Borne P, Zamorano JL, Achenbach S, Baumgartner H, Bax JJ, Bueno H, Dean V, Deaton C, Erol C, Fagard R, Ferrari R, Hasdai D, Hoes AW, Kirchhof P, Knuuti J, Kolh P, Lancellotti P, Linhart A, Nihoyannopoulos P, Piepoli MF, Ponikowski P, Sirnes PA, Tamargo JL, Tendera M, Torbicki A, Wijns W, Windecker S, Clement DL, Coca A, Gillebert TC, Tendera M, Rosei EA, Ambrosioni E, Anker SD, Bauersachs J, Hitij JB, Caulfield M, De Buyzere M, De Geest S, Derumeaux GA, Erdine S, Farsang C, Funck-Brentano C, Gerc V, Germano G, Gielen S, Haller H, Hoes AW, Jordan J, Kahan T, Komajda M, Lovic D, Mahrholdt H, Olsen MH, Ostergren J, Parati G, Perk J, Polonia J, Popescu BA, Reiner Z, Ryden L, Sirenko Y, Stanton A, Struijker-Boudier H, Tsioufis C, van de Borne P, Vlachopoulos C, Volpe M, Wood DA. 2013 ESH/ESC guidelines for the management of arterial hypertension: The Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Eur Heart J 2013; 34: 2159-2219
  • 62 Walsh JP, Bremner AP, Bulsara MK, O'Leary P, Leedman PJ, Feddema P, Michelangeli V. Subclinical thyroid dysfunction and blood pressure: A community-based study. Clin Endocrinol (Oxf) 2006; 65: 486-491
  • 63 Kaminski G, Makowski K, Michalkiewicz D, Kowal J, Ruchala M, Szczepanek E, Gielerak G. The influence of subclinical hyperthyroidism on blood pressure, heart rate variability, and prevalence of arrhythmias. Thyroid 2012; 22: 454-460
  • 64 Volzke H, Alte D, Dorr M, Wallaschofski H, John U, Felix SB, Rettig R. The association between subclinical hyperthyroidism and blood pressure in a population-based study. J Hypertens 2006; 24: 1947-1953
  • 65 Volzke H, Ittermann T, Schmidt CO, Dorr M, John U, Wallaschofski H, Stricker BH, Felix SB, Rettig R. Subclinical hyperthyroidism and blood pressure in a population-based prospective cohort study. Eur J Endocrinol 2009; 161: 615-621
  • 66 Biondi B, Palmieri EA, Fazio S, Cosco C, Nocera M, Sacca L, Filetti S, Lombardi G, Perticone F. Endogenous subclinical hyperthyroidism affects quality of life and cardiac morphology and function in young and middle-aged patients. J Clin Endocrinol Metab 2000; 85: 4701-4705
  • 67 Petretta M, Bonaduce D, Spinelli L, Vicario ML, Nuzzo V, Marciano F, Camuso P, De Sanctis V, Lupoli G. Cardiovascular haemodynamics and cardiac autonomic control in patients with subclinical and overt hyperthyroidism. Eur J Endocrinol 2001; 145: 691-696
  • 68 Casu M, Cappi C, Patrone V, Repetto E, Giusti M, Minuto F, Murialdo G. Sympatho-vagal control of heart rate variability in patients treated with suppressive doses of L-thyroxine for thyroid cancer. Eur J Endocrinol 2005; 152: 819-824
  • 69 Faber J, Wiinberg N, Schifter S, Mehlsen J. Haemodynamic changes following treatment of subclinical and overt hyperthyroidism. Eur J Endocrinol 2001; 145: 391-396
  • 70 Bengtsson D, Brudin L, Wanby P, Carlsson M. Previously unknown thyroid dysfunction in patients with acute ischemic stroke. Acta Neurol Scand 2012; 126: 98-102
  • 71 Cappola AR, Fried LP, Arnold AM, Danese MD, Kuller LH, Burke GL, Tracy RP, Ladenson PW. Thyroid status, cardiovascular risk, and mortality in older adults. JAMA 2006; 295: 1033-1041
  • 72 Collet TH, Gussekloo J, Bauer DC, den Elzen WP, Cappola AR, Balmer P, Iervasi G, Asvold BO, Sgarbi JA, Volzke H, Gencer B, Maciel RM, Molinaro S, Bremner A, Luben RN, Maisonneuve P, Cornuz J, Newman AB, Khaw KT, Westendorp RG, Franklyn JA, Vittinghoff E, Walsh JP, Rodondi N. Thyroid Studies C . Subclinical hyperthyroidism and the risk of coronary heart disease and mortality. Arch Intern Med 2012; 172: 799-809
  • 73 Drechsler C, Schneider A, Gutjahr-Lengsfeld L, Kroiss M, Carrero JJ, Krane V, Allolio B, Wanner C, Fassnacht M. Thyroid function, cardiovascular events, and mortality in diabetic hemodialysis patients. Am J Kidney Dis 2014; 63: 988-996
  • 74 Schultz M, Kistorp C, Raymond I, Dimsits J, Tuxen C, Hildebrandt P, Faber J. Cardiovascular events in thyroid disease: A population based, prospective study. Horm Metab Res 2011; 43: 653-659
  • 75 Selmer C, Olesen JB, Hansen ML, von Kappelgaard LM, Madsen JC, Hansen PR, Pedersen OD, Faber J, Torp-Pedersen C, Gislason GH. Subclinical and overt thyroid dysfunction and risk of all-cause mortality and cardiovascular events: A large population study. J Clin Endocrinol Metab 2014; 99: 2372-2382
  • 76 Wollenweber FA, Zietemann V, Gschwendtner A, Opherk C, Dichgans M. Subclinical hyperthyroidism is a risk factor for poor functional outcome after ischemic stroke. Stroke 2013; 44: 1446-1448
  • 77 Ahmed A. American College of Cardiology/American Heart Association Chronic Heart Failure Evaluation and Management guidelines: Relevance to the geriatric practice. J Am Geriatr Soc 2003; 51: 123-126
  • 78 Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JG, Coats AJ, Falk V, Gonzalez-Juanatey JR, Harjola VP, Jankowska EA, Jessup M, Linde C, Nihoyannopoulos P, Parissis JT, Pieske B, Riley JP, Rosano GM, Ruilope LM, Ruschitzka F, Rutten FH, van der Meer P. Authors/Task Force M . 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: The Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC)Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J 2016; 37: 2129-2200
  • 79 Wang W, Guan H, Gerdes AM, Iervasi G, Yang Y, Tang YD. Thyroid Status, Cardiac Function, and Mortality in Patients With Idiopathic Dilated Cardiomyopathy. J Clin Endocrinol Metab 2015; 100: 3210-3218
  • 80 Nanchen D, Gussekloo J, Westendorp RG, Stott DJ, Jukema JW, Trompet S, Ford I, Welsh P, Sattar N, Macfarlane PW, Mooijaart SP, Rodondi N, de Craen AJ. Group P . Subclinical thyroid dysfunction and the risk of heart failure in older persons at high cardiovascular risk. J Clin Endocrinol Metab 2012; 97: 852-861
  • 81 Gencer B, Collet TH, Virgini V, Bauer DC, Gussekloo J, Cappola AR, Nanchen D, den Elzen WP, Balmer P, Luben RN, Iacoviello M, Triggiani V, Cornuz J, Newman AB, Khaw KT, Jukema JW, Westendorp RG, Vittinghoff E, Aujesky D, Rodondi N. Thyroid Studies C . Subclinical thyroid dysfunction and the risk of heart failure events: An individual participant data analysis from 6 prospective cohorts. Circulation 2012; 126: 1040-1049
  • 82 Rodondi N, Bauer DC, Cappola AR, Cornuz J, Robbins J, Fried LP, Ladenson PW, Vittinghoff E, Gottdiener JS, Newman AB. Subclinical thyroid dysfunction, cardiac function, and the risk of heart failure. The Cardiovascular Health study. J Am Coll Cardiol 2008; 52: 1152-1159
  • 83 Asvold BO, Bjoro T, Platou C, Vatten LJ. Thyroid function and the risk of coronary heart disease: 12-year follow-up of the HUNT study in Norway. Clin Endocrinol (Oxf) 2012; 77: 911-917
  • 84 Parle JV, Maisonneuve P, Sheppard MC, Boyle P, Franklyn JA. Prediction of all-cause and cardiovascular mortality in elderly people from one low serum thyrotropin result: A 10-year cohort study. Lancet 2001; 358: 861-865
  • 85 Haentjens P, Van Meerhaeghe A, Poppe K, Velkeniers B. Subclinical thyroid dysfunction and mortality: An estimate of relative and absolute excess all-cause mortality based on time-to-event data from cohort studies. Eur J Endocrinol 2008; 159: 329-341
  • 86 Ochs N, Auer R, Bauer DC, Nanchen D, Gussekloo J, Cornuz J, Rodondi N. Meta-analysis: subclinical thyroid dysfunction and the risk for coronary heart disease and mortality. Ann Intern Med 2008; 148: 832-845
  • 87 Volzke H, Schwahn C, Wallaschofski H, Dorr M. Review: The association of thyroid dysfunction with all-cause and circulatory mortality: Is there a causal relationship?. J Clin Endocrinol Metab 2007; 92: 2421-2429
  • 88 Singh S, Duggal J, Molnar J, Maldonado F, Barsano CP, Arora R. Impact of subclinical thyroid disorders on coronary heart disease, cardiovascular and all-cause mortality: a meta-analysis. Int J Cardiol 2008; 125: 41-48
  • 89 Surks MI, Ortiz E, Daniels GH, Sawin CT, Col NF, Cobin RH, Franklyn JA, Hershman JM, Burman KD, Denke MA, Gorman C, Cooper RS, Weissman NJ. Subclinical thyroid disease: scientific review and guidelines for diagnosis and management. JAMA 2004; 291: 228-238
  • 90 Selmer C, Olesen JB, Hansen ML, Lindhardsen J, Olsen AM, Madsen JC, Faber J, Hansen PR, Pedersen OD, Torp-Pedersen C, Gislason GH. The spectrum of thyroid disease and risk of new onset atrial fibrillation: a large population cohort study. BMJ 2012; 345: e7895
  • 91 Goichot B, Caron P, Landron F, Bouee S. Clinical presentation of hyperthyroidism in a large representative sample of outpatients in France: relationships with age, aetiology and hormonal parameters. Clin Endocrinol (Oxf) 2016; 84: 445-451
  • 92 Poola R, Mathiason MA, Caplan RH. A retrospective study of the natural history of endogenous subclinical hyperthyroidism. WMJ 2011; 110: 277-280
  • 93 Duarte GC, Tomimori EK, Camargo RY, Rubio IG, Wajngarten M, Rodrigues AG, Knobel M, Medeiros-Neto G. The prevalence of thyroid dysfunction in elderly cardiology patients with mild excessive iodine intake in the urban area of Sao Paulo. Clinics (Sao Paulo) 2009; 64: 135-142
  • 94 Klein Hesselink EN, Lefrandt JD, Schuurmans EP, Burgerhof JG, Groen B, Gansevoort RT, van der Horst-Schrivers AN, Dullaart RP, Van Gelder IC, Brouwers AH, Rienstra M, Links TP. Increased risk of atrial fibrillation after treatment for differentiated thyroid carcinoma. J Clin Endocrinol Metab 2015; 100: 4563-4569