The Clinical Significance of Subclinical Thyroid Dysfunction

Biondi, Bernadette; Cooper, David S.

doi:10.1210/er.2006-0043

Cited by 1,418Thyroid Disorders and TreatmentsThyroid and Parathyroid SurgeryThyroid Cancer Diagnosis and Treatment

The Clinical Significance of Subclinical Thyroid Dysfunction

Biondi, Bernadette, Cooper, David S.·2008·Endocrine Reviews

DOI 10.1210/er.2006-0043

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Abstract

Subclinical thyroid disease (SCTD) is defined as serum free T(4) and free T(3) levels within their respective reference ranges in the presence of abnormal serum TSH levels. SCTD is being diagnosed more frequently in clinical practice in young and middle-aged people as well as in the elderly. However, the clinical significance of subclinical thyroid dysfunction is much debated. Subclinical hyper- and hypothyroidism can have repercussions on the cardiovascular system and bone, as well as on other organs and systems. However, the treatment and management of SCTD and population screening are controversial despite the potential risk of progression to overt disease, and there is no consensus on the thyroid hormone and thyrotropin cutoff values at which treatment should be contemplated. Opinions differ regarding tissue effects, symptoms, signs, and cardiovascular risk. Here, we critically review the data on the prevalence and progression of SCTD, its tissue effects, and its prognostic implications. We also examine the mechanisms underlying tissue alterations in SCTD and the effects of replacement therapy on progression and tissue parameters. Lastly, we address the issue of the need to treat slight thyroid hormone deficiency or excess in relation to the patient's age.

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Cardiac adverse events including tachycardia, palpitations and atrial fibrillation arise from increased myocardial oxygen consumption and enhanced beta-adrenergic sensitivity.
“Cardiac AEs, including tachycardia, palpitations and atrial fibrillation, arise from increased myocardial oxygen consumption and enhanced β‐adrenergic sensitivity.”
From Risk of cardiac, neuropsychiatric and musculoskeletal adverse events with levothyroxine: Systematic review (2026) · cites this paper as [5]
Serum free T4 and free T3 levels are generally normal to low-normal in people with central causes of low serum TSH.
“Serum free T 4 and free T 3 levels are generally normal to low-normal in people with the latter conditions [3,5,18] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
Subnormal serum TSH concentrations are frequently observed in black people and in some healthy cigarette smokers.
“Finally, subnormal serum TSH concentrations are frequently observed in black people and in some healthy cigarette smokers [3,5,25] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
The degree of TSH suppression is the best parameter for predicting the progression from subclinical to overt hyperthyroidism.
“The degree of TSH suppression is the best parameter for predicting the progression from subclinical to overt hyperthyroidism [3,5,18,31] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
The observed changes in type I interferon activity and thyroid hormone signaling with aging are consistent with prior literature and our differential expression analysis.
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From Murine single-cell RNA-seq reveals cell-identity- and tissue-specific trajectories of aging (2019) · cites this paper as Biondi and Cooper 2008

Differences in the degree of TSH suppression, causes of subclinical hyperthyroidism, patient age, and duration of TSH suppression may influence the adverse consequences of endogenous subclinical hyperthyroidism.
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From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
Subclinical hyperthyroidism may progress to overt hyperthyroidism and may be associated with increased cardiovascular and skeletal risk.
“SHyper may progress to overt hyperthyroidism and may be associated with increased cardiovascular and skeletal risk [3,5,18] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
Endogenous subclinical hyperthyroidism is most commonly due to Graves' disease, toxic adenoma, and toxic multinodular goitre.
“Endogenous SHyper is most commonly due to Graves' disease (GD), toxic adenoma (TA) and toxic multinodular goitre (MNG) [3,5] ( table 1 ).”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
Suppression of TSH may be iatrogenic due to thyroid hormone overtreatment, either intentionally, unintentionally, or surreptitiously.
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From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [3]
Increased arterial stiffness and a low renin state contribute to blood pressure and vascular dysregulation due to the lack of normal vasodilatory effects of triiodothyronine.
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From Thyroid Hormones and Cardiovascular Function and Diseases (2018) · cites this paper as [4]
Trials of levothyroxine in subclinical hypothyroidism using surrogate markers have shown improvement in left ventricular function, vascular endothelial function, atherogenic lipid particles, or cardiac mitochondrial function.
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From Thyroid Hormones and Cardiovascular Function and Diseases (2018) · cites this paper as [4]
Definitions of hypothyroidism or hyperthyroidism were adjusted, introducing new laboratory-based and TSH-derived disease entities of subclinical hypothyroidism and hyperthyroidism, which are defined by an abnormal TSH level while FT3 and FT4 still dwell within their reference ranges.
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Biondi, B., Fazio, S., Carella, C., Amato, G., Cittadini, A., Lupoli, G., Saccà, L., Bellastella, A., & Lombardi, G. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.2.8345037 · Cited by 237 · see citing works
Self-citation
Flow-Mediated, Endothelium-Dependent Vasodilatation Is Impaired in Subjects with Hypothyroidism, Borderline Hypothyroidism, and High-Normal Serum Thyrotropin (TSH) Values
Lekakis, J. P., Papamichael, C. M., Alevizaki, M. K., Gd, P., MARAFELIA, P., Mantzos, J. D., Stamatelopoulos, S., & Koutras, D. A. (1997) · Thyroid · doi:10.1089/thy.1997.7.411 · Cited by 236 · see citing works
Thyroid Diseases and Cerebrovascular Disease
Squizzato, A., Gerdes, V. E. A., Brandjes, D. P. M., Büller, H. R., & Stam, J. (2005) · Stroke · doi:10.1161/01.str.0000181772.78492.07 · Cited by 236 · see citing works
New Reference Intervals for Thyrotropin and Thyroid Hormones Based on National Academy of Clinical Biochemistry Criteria and Regular Ultrasonography of the Thyroid
Kratzsch, J., Fiedler, G. M., Leichtle, A., Brügel, M., Buchbinder, S., Otto, L., Sabri, O., Matthes, G., & Thiery, J. (2005) · Clinical Chemistry · doi:10.1373/clinchem.2004.047399 · Cited by 235 · see citing works
Complex alteration of thyroid function in healthy centenarians.
Mariotti, S., Barbesino, G., Caturegli, P., Bartalena, L., Sansoni, P., Fagnoni, F., Monti, D., Fagiolo, U., Franceschi, C., & Pinchera, A. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.5.8077303 · Cited by 234 · see citing works
Consensus statement for good practice and audit measures in the management of hypothyroidism and hyperthyroidism
Vanderpump, M. P. J., Ahlquist, J., Franklyn, J., & Clayton, R. (1996) · BMJ · doi:10.1136/bmj.313.7056.539 · Cited by 233 · see citing works
Subclinical Hyperthyroidism
Toft, A. D. (2001) · New England Journal of Medicine · doi:10.1056/nejmcp010145 · Cited by 231 · see citing works
The Treatment of Subclinical Hypothyroidism Is Seldom Necessary
Chu, J. W., & Crapo, L. M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.10.7961 · Cited by 231 · see citing works
A therapeutic dilemma: suppressive doses of thyroxine significantly reduce bone mineral measurements in both premenopausal and postmenopausal women with thyroid carcinoma.
Diamond, T. H., Nery, L., & Hales, I. B. (1991) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jcem-72-6-1184 · Cited by 225 · see citing works
A 6-month randomized trial of thyroxine treatment in women with mild subclinical hypothyroidism
Kong, W. M., Sheikh, M. H., Lumb, P. J., Freedman, D. B., Crook, M. A., Doré, C. J., & Finer, N. (2002) · The American Journal of Medicine · doi:10.1016/s0002-9343(02)01022-7 · Cited by 223 · see citing works
Differences in the Signs and Symptoms of Hyperthyroidism in Older and Younger Patients
Trivalle, C., Doucet, J., Chassagne, P., Landrin, I., Kadri, N., Ménard, J.-F., & Bercoff, E. (1996) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1996.tb05637.x · Cited by 222 · see citing works
Thyroid-hormone therapy and thyroid cancer: a reassessment
Biondi, B., Filetti, S., & Schlumberger, M. J. (2005) · Nature Clinical Practice Endocrinology &#38 Metabolism · doi:10.1038/ncpendmet0020 · Cited by 221 · see citing works
Self-citation
Subclinical hyperthyroidism: clinical features and treatment options
Biondi, B., Palmieri, E. A., Klain, M., Schlumberger, M., Filetti, S., & Lombardi, G. (2005) · European Journal of Endocrinology · doi:10.1530/eje.1.01809 · Cited by 217 · see citing works
Self-citation
Long-term thyroxine treatment and bone mineral density.
Franklyn, J., Betteridge, J., Daykin, J., Oates, G., Parle, J., Heath, D., Sheppard, M., Holder, R., & Lilley, J. (1992) · The Lancet · doi:10.1016/0140-6736(92)92423-d · Cited by 216 · see citing works
Does treatment withl-thyroxine influence health status in middle-aged and older adults with subclinical hypothyroidism?
Jaeschke, R., Guyatt, G. H., Gerstein, H. C., Patterson, C., Molloy, W., Cook, D., Harper, S., Griffith, L. E., & Carbotte, R. M. (1996) · Journal of General Internal Medicine · doi:10.1007/bf02598988 · Cited by 216 · see citing works
Association between blood pressure and serum thyroid-stimulating hormone concentration within the reference range: a population-based study
Åsvold, B. O., Bjøro, T., Nilsen, T. I. L., & Vatten, L. J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2208 · Cited by 215 · see citing works
The Association Between Lipid Levels and the Risks of Incident Myocardial Infarction, Stroke, and Total Mortality: The Cardiovascular Health Study
Psaty, B. M., Anderson, M. L., Kronmal, R. A., Tracy, R. P., Orchard, T. J., Fried, L. P., Lumley, T., Robbins, J. A., Burke, G. L., Newman, A. B., et al. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52455.x · Cited by 211 · see citing works
Is there a need to redefine the upper normal limit of TSH?
Brabant, G., Beck-Peccoz, P., Jarzab, B., Laurberg, P., Orgiazzi, J., Szabolcs, I., Weetman, A. P., & Wiersinga, W. M. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02136 · Cited by 211 · see citing works
Subclinical Hypothyroidism and the Risk of Hypercholesterolemia
Hueston, W. J. (2004) · The Annals of Family Medicine · doi:10.1370/afm.79 · Cited by 210 · see citing works
An association between depression, anxiety and thyroid function – a clinical fact or an artefact?
Engum, A., Bjøro, T., Mykletun, A., & Dahl, A. A. (2002) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2002.01250.x · Cited by 208 · see citing works
The development of ischemic heart disease in relation to autoimmune thyroid disease in a 20-year follow-up study of an English community.
Vanderpump, M. P. J., Tunbridge, W. M. G., French, J. M., Appleton, D. R., Bates, D., Clark, F., Evans, J. G., Rodgers, H., Tunbridge, F. K. E., & Young, E. T. (1996) · PubMed · doi:10.1089/thy.1996.6.155 · Cited by 207 · see citing works
Evolution of Toxicity in Solitary Nontoxic Autonomously Functioning Thyroid Nodules
Hamburger, J. I. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-50-6-1089 · Cited by 206 · see citing works
Subclinical hypothyroidism: neurobehavioral features and beneficial effect of l-thyroxine treatment
Monzani, F., Guerra, P., Caracciol, N., Pruneti, C. A., Puccil, E., Luisit, M., & Baschieri, L. (1993) · Journal of Molecular Medicine · doi:10.1007/bf00186625 · Cited by 204 · see citing works
Natural history of thyroid abnormalities: Prevalence, incidence, and regression of thyroid diseases in adolescents and young adults
Rallison, M. L., DOBYNS, B. M., Meikle, A. W., Bishop, M., Lyon, J. L., & Stevens, W. (1991) · The American Journal of Medicine · doi:10.1016/0002-9343(91)90153-o · Cited by 203 · see citing works
Thyroid failure in the elderly. Microsomal antibodies as discriminant for therapy
Rosenthal, M. J. (1987) · JAMA · doi:10.1001/jama.258.2.209 · Cited by 203 · see citing works
The Effects of Lithium Therapy on Thyroid and Thyrotropin-Releasing Hormone
Lazarus, J. H. (1998) · Thyroid · doi:10.1089/thy.1998.8.909 · Cited by 201 · see citing works
A Comparison of Short-Term Changes in Health-Related Quality of Life in Thyroid Carcinoma Patients Undergoing Diagnostic Evaluation with Recombinant Human Thyrotropin Compared with Thyroid Hormone Withdrawal
Schroeder, P. R., Haugen, B. R., Pacini, F., Reiners, C., Schlumberger, M. J., Sherman, S. I., Cooper, D. S., Schuff, K. G., Braverman, L. E., Skarulis, M. C., et al. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2064 · Cited by 198 · see citing works
Self-citation
Thyrotropin secretion in patients with central hypothyroidism: Evidence for reduced biological activity of immunoreactive thyrotropin
FAGLIA, G., BITENSKY, L., PINCHERA, A., FERRARI, C., PARACCHI, A., BECK-PECCOZ, P., AMBROSI, B., & SPADA, A. (1979) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-48-6-989 · Cited by 197 · see citing works
Low-Grade Systemic Inflammation Causes Endothelial Dysfunction in Patients with Hashimoto’s Thyroiditis
Taddei, S., Caraccio, N., Virdis, A., Dardano, A., Versari, D., Ghiadoni, L., Ferrannini, E., Salvetti, A., & Monzani, F. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1075 · Cited by 196 · see citing works
Long-Term Changes in Nodular Goiter: A 5-Year Prospective Randomized Trial of Levothyroxine Suppressive Therapy for Benign Cold Thyroid Nodules
Papini, E., Petrucci, L., Guglielmi, R., Panunzi, C., Rinaldi, R., Bacci, V., Crescenzi, A., Nardi, F., Fabbrini, R., & Pacella, C. M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.3.4615 · Cited by 194 · see citing works
Screening for Mild Thyroid Failure at the Periodic Health Examination
Danese, M. D. (1996) · JAMA · doi:10.1001/jama.1996.03540040029029 · Cited by 193 · see citing works
Reference Intervals of Serum Thyroid Function Tests in a Previously Iodine-Deficient Area
Völzke, H., Alte, D., Kohlmann, T., Lüdemann, J., Nauck, M., John, U., & Meng, W. (2005) · Thyroid · doi:10.1089/thy.2005.15.279 · Cited by 192 · see citing works
Subclinical Hypothyroidism may be Associated with Elevated High-sensitive C-Reactive Protein (Low Grade Inflammation) and Fasting Hyperinsulinemia
Tuzcu, A., Bahçeci, M., Gökalp, D., Tüzün, Y., & GUNES, K. (2005) · Endocrine Journal · doi:10.1507/endocrj.52.89 · Cited by 190 · see citing works
The Relationship between Thyrotropin and Low Density Lipoprotein Cholesterol Is Modified by Insulin Sensitivity in Healthy Euthyroid Subjects
Bakker, S. J. L., ter Maaten, J. C., Popp‐Snijders, C., Slaets, J. P. J., Heine, R. J., & Gans, R. O. B. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.3.7324 · Cited by 190 · see citing works
Are Detection and Treatment of Thyroid Insufficiency in Pregnancy Feasible?
Mandel, S. J., Spencer, C. A., & Hollowell, J. G. (2005) · Thyroid · doi:10.1089/thy.2005.15.44 · Cited by 185 · see citing works
Psychopathological and cognitive features in subclinical hypothyroidism
Baldini, I., Vita, A., Mauri, M. C., Amodei, V., Carrisi, M., Bravin, S., & CANTALAMESSA, L. (1997) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(97)00089-4 · Cited by 184 · see citing works
High Attributable Risk of Elevated C-Reactive Protein Level to Conventional Coronary Heart Disease Risk Factors
Miller, M. J., Zhan, M., & Havas, S. (2005) · Archives of Internal Medicine · doi:10.1001/archinte.165.18.2063 · Cited by 184 · see citing works
STATISTICAL METHODS APPLIED TO THE DIAGNOSIS OF HYPOTHYROLDISM
Billewicz, W. Z., CHAPMAN, R. S., Crooks, J., DAY, M. E., GOSSAGE, J., Wayne, E. J., & YOUNG, J. A. (1969) · QJM · doi:10.1093/oxfordjournals.qjmed.a067179 · Cited by 183 · see citing works
Relationship between Thyrotropin and Thyroxine Changes during Recovery from Severe Hypothyroxinemia of Critical Illness*
Hamblin, P. S., Dyer, S. A., MOHR, V. S., GRAND, B. A. L., Lim, C., Tuxen, D. V., Topliss, D. J., & Stockigt, J. R. (1986) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-62-4-717 · Cited by 182 · see citing works
LIPID PROFILES AND CARDIOVASCULAR DISEASE IN THE WHICKHAM AREA WITH PARTICULAR REFERENCE TO THYROID FAILURE
Tunbridge, W. M. G., Evered, D. C., Hall, R., Appleton, D. R., BREWIS, M., CLARK, F., Evans, J. G., Young, E. T., Bird, T., & Smith, P. (1977) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1977.tb01341.x · Cited by 177 · see citing works
Effect of thyroid substitution on hypercholesterolaemia in patients with subclinical hypothyroidism: a reanalysis of intervention studies
Tanis, B. C., Westendorp, R. G. J., & Smelt, A. H. M. (1996) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1996.739560.x · Cited by 177 · cited 2× · see citing works
“4 mmol/liter (15 mg/dl) independently of the initial plasma level; however, plasma levels remained elevated in most patients (267).”
Background
The Effects of Early Antithyroid Therapy for Endogenous Subclinical Hyperthyroidism in Clinical and Heart Abnormalities
Sgarbi, J. A., Villaça, F. G., Garbeline, B., Villar, H. E., & Romaldini, J. H. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021046 · Cited by 177 · see citing works
The Aging Thyroid
Sawin, C. T. (1979) · JAMA · doi:10.1001/jama.1979.03300030019013 · Cited by 176 · see citing works
Health-related quality of life in patients with thyroid disorders
Bianchi, G. P., Zaccheroni, V., Solaroli, E., Vescini, F., Cerutti, R., Zoli, M., & Marchesini, G. (2004) · Quality of Life Research · doi:10.1023/b:qure.0000015315.35184.66 · Cited by 174 · see citing works
Serum lipid levels in relation to serum thyroid-stimulating hormone and the effect of thyroxine treatment on serum lipid levels in subjects with subclinical hypothyroidism: the Tromsø Study
IQBAL, A., JORDE, R., & FIGENSCHAU, Y. (2006) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2006.01652.x · Cited by 174 · see citing works
Do traditional symptoms of hypothyroidism correlate with biochemical disease?
Canaris, G. J., Steiner, J. F., & Ridgway, E. C. (1997) · Journal of General Internal Medicine · doi:10.1046/j.1525-1497.1997.07109.x · Cited by 172 · see citing works
Effects of thyroid hormone on cardiac size and myosin content of the heterotopically transplanted rat heart.
Klein, I. L., & Hong, C. (1986) · Journal of Clinical Investigation · doi:10.1172/jci112488 · Cited by 171 · see citing works
Bone mineral density in patients with endogenous subclinical hyperthyroidism: Is this thyroid status a risk factor for osteoporosis?
Földes, J., Tarján, G., Szathmari, M., Varga, F., Krasznai, I., & Horvath, C. (1993) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1993.tb02403.x · Cited by 170 · see citing works
Lack of association between serum TSH or free T4 and body mass index in euthyroid subjects
Manji, N., Boelaert, K., Sheppard, M. C., Holder, R. L., Gough, S. C. L., & Franklyn, J. A. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02433.x · Cited by 167 · see citing works
High Prevalence of Autoimmune Thyroiditis in Schoolchildren After Elimination of Iodine Deficiency in Northwestern Greece
Zois, C. D., Stavrou, I., Kalogera, C., Svarna, E., Dimoliatis, I., Seferiadis, K. I., & Tsatsoulis, A. A. (2003) · Thyroid · doi:10.1089/105072503322021151 · Cited by 166 · see citing works
Impaired Action of Thyroid Hormone Associated with Smoking in Women with Hypothyroidism
Müller-Stich, B. P., Zulewski, H., Huber, P., Ratcliffe, J. G., & Staub, J.-J. (1995) · New England Journal of Medicine · doi:10.1056/nejm199510123331503 · Cited by 166 · see citing works

Flagged first, then by citations

8 of the 539 references couldn’t be matched to a known paper.

Sorted by citations

Guidelines for the Treatment of Hypothyroidism: Prepared by the American Thyroid Association Task Force on Thyroid Hormone Replacement
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., et al. (2014) · Thyroid® · doi:10.1089/thy.2014.0028 · Cited by 1,928 · see citing works
“It is well known that in mild primary hypothyroidism, serum T3 is kept normal in the face of a low serum T4 and mildly elevated TSH (4).”
Self-citation
Subclinical Hypothyroidism and the Risk of Coronary Heart Disease and Mortality
Rodondi, N., den Elzen, W. P. J., Bauer, D. C., Cappola, A. R., Razvi, S., Walsh, J. P., Åsvold, B. O., Iervasi, G., Imaizumi, M., Collet, T.-H., et al. (2010) · JAMA · doi:10.1001/jama.2010.1361 · Cited by 1,216 · see citing works
The epidemiology of thyroid disease
Vanderpump, M. P. J. (2011) · British Medical Bulletin · doi:10.1093/bmb/ldr030 · Cited by 1,179 · see citing works
Biomarkers of Nutrition for Development—Folate Review
Bailey, L. B., Stover, P. J., McNulty, H., Fenech, M. F., Gregory, J. F., Mills, J. L., Pfeiffer, C. M., Fazili, Z., Zhang, M., Ueland, P. M., et al. (2015) · Journal of Nutrition · doi:10.3945/jn.114.206599 · Cited by 1,147 · see citing works
Iodine Deficiency
Zimmermann, M. B. (2009) · Endocrine Reviews · doi:10.1210/er.2009-0011 · Cited by 1,071 · see citing works
Subclinical thyroid disease
Cooper, D. S., & Biondi, B. (2012) · The Lancet · doi:10.1016/s0140-6736(11)60276-6 · Cited by 1,039 · see citing works
Self-citation
2013 ETA Guideline: Management of Subclinical Hypothyroidism
Pearce, S. H. S., Brabant, G., Duntas, L. H., Monzani, F., Peeters, R. P., Razvi, S., & Wemeau, J.-L. (2013) · European Thyroid Journal · doi:10.1159/000356507 · Cited by 877 · see citing works
Thyroid hormones and cardiovascular disease
Jabbar, A., Pingitore, A., Pearce, S. H. S., Zaman, A., Iervasi, G., & Razvi, S. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2016.174 · Cited by 729 · see citing works
Subclinical Hypothyroidism: A Review
Biondi, B., Cappola, A. R., & Cooper, D. S. (2019) · JAMA · doi:10.1001/jama.2019.9052 · Cited by 604 · see citing works
Self-citation
Characteristics of Secondary, Primary, and Compensated Hypogonadism in Aging Men: Evidence from the European Male Ageing Study
Tajar, A., Forti, G., O'Neill, T. W., Lee, D. M., Silman, A. J., Finn, J. D., Bartfai, G., Boonen, S., Casanueva, F. F., Giwercman, A., et al. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1796 · Cited by 604 · see citing works
Thyroid dysfunction and diabetes mellitus: two closely associated disorders
Biondi, B., Kahaly, G. J., & Robertson, R. P. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00163 · Cited by 598 · see citing works
Self-citation
Subclinical hyperthyroidism and the risk of coronary heart disease and mortality
Collet, T.-H., Gussekloo, J., Bauer, D. C., den Elzen, W. P. J., Cappola, A. R., Balmer, P., Iervasi, G., Åsvold, B. O., Sgarbi, J. A., Völzke, H., et al. (2012) · Archives of Internal Medicine · doi:10.1001/archinternmed.2012.402 · Cited by 572 · see citing works
Subclinical Thyroid Dysfunction and the Risk of Heart Failure Events: An Individual Participant Data Analysis From 6 Prospective Cohorts
Gencer, B., Collet, T.-H., Virgini, V., Bauer, D. C., Gussekloo, J., Cappola, A. R., Nanchen, D., den Elzen, W. P. J., Balmer, P., Luben, R. N., et al. (2012) · Circulation · doi:10.1161/circulationaha.112.096024 · Cited by 517 · see citing works
Thyroid Hormones and Cardiovascular Function and Diseases
Razvi, S., Jabbar, A., Pingitore, A., Danzi, S., Biondi, B., Klein, I., Peeters, R., Zaman, A., & Iervasi, G. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2018.02.045 · Cited by 515 · see citing works
Self-citation
Iodine intake as a determinant of thyroid disorders in populations
Laurberg, P., Cerqueira, C., Ovesen, L., Rasmussen, L. B., Perrild, H., Andersen, S., Pedersen, I. B., & Carlé, A. (2010) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2009.08.013 · Cited by 507 · see citing works
Breast cancer survivorship: a comprehensive review of long-term medical issues and lifestyle recommendations
Bodai, B. I., & Tuso, P. (2015) · The Permanente Journal · doi:10.7812/tpp/14-241 · Cited by 397 · see citing works
Effects of Thyroid Dysfunction on Lipid Profile
Rizos, C. V., Elisaf, M., & Liberopoulos, E. N. (2011) · The Open Cardiovascular Medicine Journal · doi:10.2174/1874192401105010076 · Cited by 403 · see citing works
Subclinical Hypothyroidism: An Update for Primary Care Physicians
Fatourechi, V. (2009) · Mayo Clinic Proceedings · doi:10.4065/84.1.65 · Cited by 376 · see citing works
Age-Related Changes in Thyroid Function: A Longitudinal Study of a Community-Based Cohort
Bremner, A. P., Feddema, P., Leedman, P. J., Brown, S. J., Beilby, J. P., Lim, E. M., Wilson, S. G., O'Leary, P. C., & Walsh, J. P. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-3020 · Cited by 336 · see citing works
The Influence of Age on the Relationship between Subclinical Hypothyroidism and Ischemic Heart Disease: A Metaanalysis
Razvi, S., Shakoor, A., Vanderpump, M., Weaver, J. U., & Pearce, S. H. S. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0167 · Cited by 330 · see citing works
Thyroid and Obesity: An Intriguing Relationship
Biondi, B. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1245 · Cited by 330 · see citing works
Self-citation
The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism
Biondi, B., Bartalena, L., Cooper, D. S., Hegedüs, L., Laurberg, P., & Kahaly, G. J. (2015) · European Thyroid Journal · doi:10.1159/000438750 · Cited by 323 · see citing works
Self-citation
Association of Depression and Anxiety Disorders With Autoimmune Thyroiditis: A Systematic Review and Meta-analysis
Siegmann, E.-M., Müller, H. H. O., Luecke, C., Philipsen, A., Kornhuber, J., & Grömer, T. W. (2018) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2018.0190 · Cited by 304 · see citing works
Non-alcoholic fatty liver disease across the spectrum of hypothyroidism
Chung, G. E., Kim, D., Kim, W. K., Yim, J. Y., Park, M. J., Kim, Y. J., Yoon, J., & Lee, H.-S. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2012.02.027 · Cited by 302 · see citing works
MECHANISMS IN ENDOCRINOLOGY: Heart failure and thyroid dysfunction
Biondi, B. (2012) · European Journal of Endocrinology · doi:10.1530/eje-12-0627 · Cited by 291 · see citing works
Self-citation
Subclinical and Overt Thyroid Dysfunction and Risk of All-Cause Mortality and Cardiovascular Events: A Large Population Study
Selmer, C., Olesen, J. B., Hansen, M. L., von Kappelgaard, L. M., Madsen, J. C., Hansen, P. R., Pedersen, O. D., Faber, J., Torp-Pedersen, C., & Gislason, G. H. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-4184 · Cited by 288 · see citing works
Benefits of Thyrotropin Suppression Versus the Risks of Adverse Effects in Differentiated Thyroid Cancer
Biondi, B., & Cooper, D. S. (2010) · Thyroid · doi:10.1089/thy.2009.0311 · Cited by 286 · see citing works
Self-citation
Biomarkers of Nutrition for Development—Iodine Review
Rohner, F., Zimmermann, M. B., Jooste, P. L., Pandav, C. S., Caldwell, K. L., Raghavan, R., & Raiten, D. J. (2014) · Journal of Nutrition · doi:10.3945/jn.113.181974 · Cited by 281 · see citing works
Genome-wide analyses identify a role for SLC17A4 and AADAT in thyroid hormone regulation
Teumer, A., Chaker, L., Groeneweg, S., Li, Y., Di Munno, C., Barbieri, C., Schultheiss, U. T., Traglia, M., Ahluwalia, T. S., Akiyama, M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06356-1 · Cited by 280 · see citing works
A Review of the Clinical Consequences of Variation in Thyroid Function Within the Reference Range
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Authors: Biondi, B., & Cooper, D. S.
Affiliations: University of Naples Federico II (IT)
Johns Hopkins University (US)
ORCID: Biondi, Bernadette
Cooper, David S.
Venue: Endocrine Reviews
Publisher: The Endocrine Society
Published: 2007-11-08
Volume: 29
Issue: 1
Pages: 76-131
ISSN: 0163-769X (ISSN-L)
1945-7189
DOI: 10.1210/er.2006-0043
OpenAlex: W2043015190
Cited by: 1,418
References: 539
Citations by year: 2026: 58 · 2025: 62 · 2024: 55 · 2023: 63 · 2022: 83 · 2021: 70 · 2020: 75 · 2019: 83 · 2018: 83 · 2017: 87 · 2016: 85 · 2015: 81 · 2014: 82 · 2013: 96 · 2012: 101
FWCI: 8.61
Type: journal article
Language: en
Open access: closed
Locations: Endocrine Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
Health Sciences › Medicine › Surgery › Thyroid and Parathyroid Surgery
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Cancer Diagnosis and Treatment
Keywords: subclinical thyroid dysfunction, subclinical hyperthyroidism, subclinical hypothyroidism, thyroid-stimulating hormone, free thyroxine, free T3, cardiovascular risk, bone metabolism, thyroid hormone replacement, thyroid screening, tissue effects
MeSH terms: Adolescent, Adult, Aged, Aged, 80 and over, Aging, Calcification, Physiologic, Cardiovascular Diseases, Child, Child, Preschool, Cognition, Diagnosis, Differential, Humans, Hyperthyroidism, Hypothalamus, Hypothyroidism, Infant, Infant, Newborn, Middle Aged, Pituitary Gland, Quality of Life, Reference Values, Risk Factors, Thyroid Diseases, Thyroid Gland, Thyrotropin, Thyroxine, Triiodothyronine, Neonatal Screening, MEDLINE

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The Clinical Significance of Subclinical Thyroid Dysfunction

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