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The sick euthyroid syndrome: changes in thyroid hormone serum parameters and hormone metabolism

Docter, R., Krenning, E. P., de Jong, M., Hennemann, G.·1993·Clinical Endocrinology

DOI 10.1111/j.1365-2265.1993.tb02401.x

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Direct determination of free thyroxin in undiluted serum by equilibrium dialysis/radioimmunoassay.
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Deiodination of Thyroid Hormone by Human Liver
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The effect of T3 and reverse T3 administration on muscle protein catabolism during fasting as measured by 3-methylhistidine excretion
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The Effects of Amiodarone on Serum Thyroid Hormones and Hepatic Thyroxine 5′-Monodeiodination in Rats*
Sogol, P. B., Hershman, J. M., REED, A. W., & DILLMANN, W. H. (1983) · Endocrinology · doi:10.1210/endo-113-4-1464 · Cited by 108
A furan fatty acid and indoxyl sulfate are the putative inhibitors of thyroxine hepatocyte transport in uremia
Lim, C. F., Bernard, B. F., de Jong, M., Docter, R., Krenning, E. P., & HENNEMANN, G. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.2.8432774 · Cited by 108
Self-citation
Regulation of the Conversion of Thyroxine to Triiodothyronine in the Perfused Rat Liver
Jennings, A. S., Ferguson, D. C., & Utiger, R. D. (1979) · Journal of Clinical Investigation · doi:10.1172/jci109623 · Cited by 105
The Role of Sulfhydryl Groups on the Impaired Hepatic 3′,3,5-Triiodothyronine Generation from Thyroxine in the Hypothyroid, Starved, Fetal, and Neonatal Rodent
Harris, A. R. C., Fang, S.-L., Hinerfeld, L., Braverman, L. E., & Vagenakis, A. G. (1979) · Journal of Clinical Investigation · doi:10.1172/jci109330 · Cited by 98
Mechanism of the Heparin-Induced Increase in the Concentration of Free Thyroxine in Plasma*
Mendel, C. M., Frost, P. H., Kunitake, S. T., & Cavalieri, R. R. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-6-1259 · Cited by 98
Observations on the factors that control the generation of triiodothyronine from thyroxine in rat liver and the nature of the defect induced by fasting.
Balsam, A., & Ingbar, S. H. (1979) · Journal of Clinical Investigation · doi:10.1172/jci109408 · Cited by 97
Reduced Plasma Thyrotropin Response to Thyrotropin Releasing Hormone After Dexamethasone Administration in Normal Subjects
Faglia, G., Ferrari, C. I., Beck‐Peccoz, P., Spada, A., TRAVAGLINI, P., & Ambrosi, B. (1973) · Hormone and Metabolic Research · doi:10.1055/s-0028-1093930 · Cited by 96
Decreased transport of thyroxine (T4), 3,3′‐5‐triiodothyronine (T3) and 3,3′,5′‐triiodothyronine (rT3) into rat hepatocytes in primary culture due to a decrease of cellular ATP content and various drugs
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Effect of fasting and acute ethanol administration on the energy state of in vivo liver as measured by 31P-NMR spectroscopy
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Estimation of Rapidly Exchangeable Cellular Thyroxine from the Plasma Disappearance Curves of Simultaneously Administered Thyroxine-131I and Albumin-125I*
Oppenheimer, J. H., Bernstein, G. S., & Hasen, J. (1967) · Journal of Clinical Investigation · doi:10.1172/jci105577 · Cited by 91
Relationship between Serum Free Fatty Acids and Thyroid Hormone Binding Inhibitor in Nonthyroid Illnesses*
CHOPRA, I. J., TECO, G. N. C., Mead, J. F., Huang, T., Beredo, A., & Solomon, D. H. (1985) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-60-5-980 · Cited by 91
Effect of Free Fatty Acids on the Concentration of Free Thyroxine in Human Serum: The Role of Albumin*
Mendel, C. M., Frost, P. H., & Cavalieri, R. R. (1986) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-63-6-1394 · Cited by 90
PLASMA THYROXINE, 3,3′,5-TRIIODOTHYRONINE AND 3,3′,5′-TRIIODOTHYRONINE DURING 3-ADRENERGIC BLOCKADE IN. HYPERTHYROIDISM
Verhoeven, R. P., Visser, T. J., Docter, R., HENNEMANN, G., & Schalekamp, M. A. D. H. (1977) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-44-5-1002 · Cited by 90
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Sulfation Preceding Deiodination of Iodothyronines in Rat Hepatocytes
Otten, M. H., Mol, J. A., & VISSER, T. J. (1983) · Science · doi:10.1126/science.6857270 · Cited by 88
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Clinical Utility and Cost-Effectiveness of Sensitive Thyrotropin Assays in Ambulatory and Hospitalized Patients
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Free Fatty Acids: A Possible Regulator of Free Thyroid Hormone Levels in Man1
Hollander, C. S., Scott, R. L., BURGESS, J. A., Rabinowitz, D. L., Merimee, T. J., & Oppenheimer, J. H. (1967) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-27-8-1219 · Cited by 84
Thyroid test abnormalities in traumatic brain Injury: Correlation with neurologic impairment and sympathetic nervous system activation
Woolf, P. D., Lee, L. A., Hamill, R. W., & McDonald, J. V. (1988) · The American Journal of Medicine · doi:10.1016/0002-9343(88)90414-7 · Cited by 83
Effects of Prolonged Dopamine Infusion on Anterior Pituitary Function in Normal Males*
Kaptein, E. M., Kletzky, O. A., Spencer, C. A., & Nicoloff, J. T. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-3-488 · Cited by 83
Subcellular Alterations Causing Reduced Hepatic Thyroxine-5'-Monodeiodinase Activity in Fasted Rats*
Kaplan, M. M. (1979) · Endocrinology · doi:10.1210/endo-104-1-58 · Cited by 83
Serum Reverse Triiodothyronine and Thyroxine Kinetics in Patients with Chronic Renal Failure*
Kaptein, E. M., Feinstein, E. I., Nicoloff, J. T., & Massry, S. G. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-57-1-181 · Cited by 82
Measurement of Thyrotropin in Clinical and Subclinical Hyperthyroidism Using a New Chemiluminescent Assay*
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Influence of Heparin on Serum Free Thyroxine1
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Are Selective Increases in Serum Thyroxine (T4)due to Iodinated Inhibitors of T4Monodeiodination Indicative of Hyperthyroidism?*
Lambert, M. J., Burger, A., Galeazzi, R. L., & Engler, D. (1982) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-55-6-1058 · Cited by 73
Improved dialysis method for free thyroxin in serum compared with five commercial radioimmunoassays in nonthyroidal illness and subjects with abnormal concentrations of thyroxin-binding globulin.
Helenius, T., & Liewendahl, K. (1983) · Clinical Chemistry · doi:10.1093/clinchem/29.5.816 · Cited by 71
Normal Free Thyroxine in Critical Nonthyroidal Illnesses Measured by Ultrafiltration of Undiluted Serum and Equilibrium Dialysis*
Surks, M. I., Hupart, K. H., Pan, C., & Shapiro, L. E. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-5-1031 · Cited by 71
Thyroid Disease and High Concentration of Serum Thyrotrophin in a Population Sample of Women
Nyström, E., Bengtsson, C., Lindquist, O., Noppa, H., Lindstedt, G., & Lundberg, P. (1981) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1981.tb09773.x · Cited by 70
Kinetic Studies of Thyroxine, 3,5,3′-Triiodothyronine, 3,3′,5′-Triiodothyronine, 3′,5′-Diiodothyronine, 3,3′-Diiodothyronine, and 3′-Monoiodothyronine in Patients with Liver Cirrhosis*
Faber, J. O., THOMSEN, H. F., Lumholtz, I. B., KIRKEGAARD, C., Siersbæk‐Nielsen, K., & Friis, T. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-53-5-978 · Cited by 70
A Competitive Ligand Binding Assay for Measurement of Thyroid Hormone-Binding Inhibitor in Serum and Tissues*
CHOPRA, I. J., Huang, T., HURD, R. E., Beredo, A., & Solomon, D. H. (1984) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-58-4-619 · Cited by 69
DIAGNOSIS OF HYPERTHYROIDISM WHEN SERUM-THYROXINE ALONE IS RAISED
Birkhäuser, M., Busset, R., Buerer, T., & Burger, A. (1977) · The Lancet · doi:10.1016/s0140-6736(77)90061-7 · Cited by 68
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Drug and Fatty Acid Effects On Serum Thyroid Hormone Binding*
Lim, C., Bai, Y., Topliss, D. J., Barlow, J., & Stockigt, J. R. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-4-682 · Cited by 67
Alterations in monodeiodination of iodothyronines in the fasting rat: Effects of reduced nonprotein sulfhydryl groups and hypothyroidism
CHOPRA, I. J. (1980) · Metabolism · doi:10.1016/0026-0495(80)90141-9 · Cited by 66
The Effect of Iopanoic Acid on the Regulation of Thyrotropin Secretion in Euthyroid Subjects*
Kleinmann, R. E., Vagenakis, A. G., & Braverman, L. E. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-2-399 · Cited by 65
Catabolic effects of thyroid hormone excess: The contribution of adrenergic activity to hypermetabolism and protein breakdown
Gelfand, R., Hutchinson-Williams, K. A., Bonde, A. A., Castellino, P., & Sherwin, R. S. (1987) · Metabolism · doi:10.1016/0026-0495(87)90168-5 · Cited by 65
Effect of thyroid hormone on metabolic adaptation to fasting
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An Inhibitor of the Binding of Thyroid Hormones to Serum Proteins Is Present in Extrathyroidal Tissues
CHOPRA, I. J., Solomon, D. H., TECO, G. N. C., & Eisenberg, J. (1982) · Science · doi:10.1126/science.7058324 · Cited by 64
Serum thyrotropin in hospitalized psychiatric patients: Evidence for hyperthyrotropinemia as measured by an ultrasensitive thyrotropin assay
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CARRIER-MEDIATED TRANSPORT OF THYROID HORMONE INTO RAT HEPATOCYTES IS RATE-LIMITING IN TOTAL CELLULAR UPTAKE AND METABOLISM
HENNEMANN, G., Krenning, E. P., Polhuys, M., Mol, J. A., Bernard, B. F., Visser, T. J., & Docter, R. (1986) · Endocrinology · doi:10.1210/endo-119-4-1870 · Cited by 63
Self-citation
Alterations in Serum Thyroid Hormones and Thyroxine-Binding Globulin in Patients with Nephrosis*
Gavin, L. A., McMahon, F. A., Castle, J. N., & Cavalieri, R. R. (1978) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-46-1-125 · Cited by 63
Protective adaptation of low serum triiodothyronine in patients with chronic renal failure
LIM, V. S., Flanigan, M. J., Zavala, D. C., & Freeman, R. M. (1985) · Kidney International · doi:10.1038/ki.1985.162 · Cited by 62
Accumulation of furancarboxylic acids in uremic serum as inhibitors of drug binding
Niwa, T., Takeda, N., Maeda, K., Shibata, M. S., & Tatematsu, A. (1988) · Clinica Chimica Acta · doi:10.1016/0009-8981(88)90250-1 · Cited by 60
Reduced Triiodothyronine Content in Liver but Not Pituitary of the Uremic Rat Model: Demonstration of Changes Compatible with Thyroid Hormone Deficiency in Liver Only*
LIM, V. S., PASSO, C., Murata, Y., FERRARI, E., Nakamura, H., & Refetoff, S. (1984) · Endocrinology · doi:10.1210/endo-114-1-280 · Cited by 60
Influence of Fasting and Refeeding on 3,3′,5′-Triiodothyronine Metabolism in Man*
LOPRESTI, J. S., GRAY, D., & NICOLOFF, J. T. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-72-1-130 · Cited by 59
Thyroxine Binding Proteins, Free Thyroxine and Thyroxine Turnover Interrelationships during Acute Infectious Illness in Man1
Lutz, J., Gregerman, R. I., Spaulding, S. W., Hornick, R. B., & Dawkins, A. T. (1972) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-35-2-230 · Cited by 57
Patients with severe nonthyroidal illness and serum thyrotropin concentrations in the hypothyroid range
Brent, G. A., Hershman, J. M., & Braunstein, G. D. (1986) · The American Journal of Medicine · doi:10.1016/0002-9343(86)90300-1 · Cited by 55
Discrepancies between serum free triiodothyronine and free thyroxin as measured by equilibrium dialysis and analog radioimmunoassay in nonthyroidal illnesses.
Liewendahl, K., Tikanoja, S., Helenius, T., & Välimäki, M. J. (1984) · Clinical Chemistry · doi:10.1093/clinchem/30.5.760 · Cited by 55
Thyroxine Transfer and Distribution in Critical Nonthyroidal Illnesses, Chronic Renal Failure, and Chronic Ethanol Abuse*
Kaptein, E. M., Kaptein, J. S., CHANG, E. I., EGODAGE, P. M., Nicoloff, J. T., & Massry, S. G. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-4-606 · Cited by 55
Effect of Interleukin-1 (IL-1) on Thyroid Hormone Metabolism in Mice: Stimulation by IL-1 of Iodothyronine 5′-Deiodinating Activity (Type I) in the Liver*
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Free thyroxine results are affected by albumin concentration and nonthyroidal illness
BAYER, M. F. (1983) · Clinica Chimica Acta · doi:10.1016/0009-8981(83)90315-7 · Cited by 54
A tentative review of recent in vitro observations of the enzymatic deiodination of iodothyronines and its possible physiological implications
Visser, T. J. (1978) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(78)90039-4 · Cited by 53
Serum thyroid hormone binding inhibitor in nonthyroidal illnesses
CHOPRA, I. J., Huang, T., Beredo, A., Solomon, D. H., & TECO, G. N. C. (1986) · Metabolism · doi:10.1016/0026-0495(86)90117-4 · Cited by 52
Impaired secretion of TSH in critically ill patients with 'low T4-syndrome'
Vierhapper, H., Laggner, A., Waldhäusl, W. K., Grubeck‐Loebenstein, B., & Kleinberger, G. (1982) · European Journal of Endocrinology · doi:10.1530/acta.0.1010542 · Cited by 52
Decreased Serum Triiodothyronine Is Associated with Increased Concentrations of Tumor Necrosis Factor
Mooradian, A. D., Reed, R. L., Osterweil, D., Schiffman, R., & Scuderi, P. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-71-5-1239 · Cited by 51
Radioimmunoassay of free thyroxine in serum: comparison with clinical findings and results of conventional thyroid-function tests.
BAYER, M. F., & McDougall, I. R. (1980) · Clinical Chemistry · doi:10.1093/clinchem/26.8.1186 · Cited by 50
Tissue thyroid hormone concentration of rat and man determined by radiommunoassay: biologic significance.
Reichlin, S., Bollinger, J., NEJAD, I., & Sullivan, P. (1973) · PubMed · Cited by 47
Factitious Elevation of Thyrotropin in a New Ultrasensitive Assay: Implications for the Use of Monoclonal Antibodies in “Sandwich” Immunoassay
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Isolation and Characterization of an Endogenous Drug-Binding Inhibitor Present in Uremic Serum
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Inhibition by Propranolol of 3,5,3′-Triiodothyronine Formation from Thyroxine in Isolated Rat Renal Tubules: An Effect Independent ofβ-Adrenergic Blockade
Heyma, P., Larkins, R. G., & Campbell, D. G. (1980) · Endocrinology · doi:10.1210/endo-106-5-1437 · Cited by 45
Peripheral Metabolism of Thyroid Hormones in Man, I. Direct Measurement of the Conversion Rate of Thyroxine to 3,5,3'-Triiodothyronine (T3) and Determination of the Peripheral and Thyroidal Production of T3
BIANCHI, R., Mariani, G., Molea, N., Vitek, F., Cazzuola, F., Carpi, A., Mazzuca, N., & Toni, M. G. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-6-1152 · Cited by 43
The distribution kinetics of triiodothyronine: studies of euthyroid subjects with decreased plasma thyroxine-binding globulin and patients with Graves' disease
Cavalieri, R. R., Steinberg, M. H., & SEARLE, G. L. (1970) · Journal of Clinical Investigation · doi:10.1172/jci106320 · Cited by 42
LOW SERUM l ‐T3 LEVELS IN THE ELDERLY SICK: PROTEIN BINDING, THYROID AND PITUITARY RESPONSIVENESS, AND REVERSE T3 CONCENTRATIONS
Burrows, A. W., COOPER, E., SHAKESPEAR, R. A., AICKIN, C. M., Fraser, S., Hesch, R. D., & Burke, C. W. (1977) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1977.tb01328.x · Cited by 42
Thyroid Hormone Metabolism in Renal Diseases1
Kaptein, E. M., Feinstein, E. I., & Massry, S. G. (2015) · Contributions to nephrology · doi:10.1159/000407070 · Cited by 41
Simultaneous Turnover Studies of Thyroxine, 3,5,3′-and 3,3′,5′-Triiodothyronine, 3,5-, 3,3′-, and 3′,5′-Diiodothyronine, and 3′-Monoiodothyronine in Chronic Renal Failure*
Faber, J. O., Heaf, J. G., KIRKEGAARD, C., Lumholtz, I. B., Siersbæk‐Nielsen, K., KØLENDORE, K., & Friis, T. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-2-211 · Cited by 41
Direct and indirect techniques for free thyroxin compared in patients with nonthyroidal illness. II. Effect of prealbumin, albumin, and thyroxin-binding globulin.
Csákó, G., ZWEIG, M. H., Glickman, J., Ruddel, M. E., & Kestner, J. (1989) · Clinical Chemistry · doi:10.1093/clinchem/35.8.1655 · Cited by 40
Limitations to the Use of a Sensitive Assay for Serum Thyrotropin in the Assessment of Thyroid Status
Ehrmann, D. A. (1989) · Archives of Internal Medicine · doi:10.1001/archinte.1989.00390020087018 · Cited by 40
Secondary Hypothyroidism in Severe Non Thyroidal Illness?
Heinen, E., Herrmann, J., Königshausen, T., & Krüskemper, H. L. (1981) · Hormone and Metabolic Research · doi:10.1055/s-2007-1019245 · Cited by 40
Transport of 3,5,3'-triiodothyronine into the perfused rat liver and subsequent metabolism are inhibited by fasting
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Pattern of Recovery of Thyroid Hormone Indices Associated with Treatment of Diabetes Mellitus*
Alexander, C. M., Kaptein, E. M., Lum, S. M. C., Spencer, C. A., Kumar, D., & Nicoloff, J. T. (1982) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-54-2-362 · Cited by 39
Treatment of dopamine-dependent shock with triiodothyronine
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Thyroid hormone binding in nonthyroid illness
Woeber, K. A., & Maddux, B. A. (1981) · Metabolism · doi:10.1016/0026-0495(81)90124-4 · Cited by 38
EFFECTS OF THREE-DAY ORAL CHOLECYSTOGRAPHY ON SERUM IODOTHYRONINES AND TSH CONCENTRATIONS: COMPARISON OF THE EFFECTS AMONG SOME CHOLECYSTOGRAPHIC AGENTS AND THE EFFECTS OF IOPANOIC ACID ON THE PITUITARY-THYROID AXIS
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THE RATIO OF THYROXINE TO THYROXINE‐BINDING GLOBULIN IN THE ASSESSMENT OF THYROID FUNCTION
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Performance criteria for appropriate characterization of "(highly) sensitive" thyrotropin assays.
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Measurement of Thyroxine Uptake from Serum by Cultured Human Hepatocytes as an Index of Thyroid Status: Reduced Thyroxine Uptake from Serum of Patients with Nonthyf oidal Illness*
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Erratum: Revised Calculations of Common Parameters of Iodothyronine Metabolism and Distribution by Noncompartmental Analysis
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Effective laboratory evaluation of thyroid status.
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Augmentation of protein degradation by l-triiodothyronine in uremia
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How sensitive are immunometric assays for thyrotropin?
McConway, M. G., Chapman, R., Beastall, G. H., Brown, E., Tillman, J., Bonar, J. A., Hutchison, A. S., Allison, T. G., Finlayson, J., & Weston, R. (1989) · Clinical Chemistry · doi:10.1093/clinchem/35.2.289 · Cited by 33
Serum Angiotensin-Converting Enzyme in Severe Nonthyroidal Illnesses Associated with Low Serum Thyroxine Concentration
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Carbohydrate in Contrast to Protein Feeding Increases the Hepatic Content of Active Thyroxine-5′-Deiodinase in the Rat*
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Inability to detect an inhibitor of thyroxine-serum protein binding in sera from patients with nonthyroid illness
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The Influence of Fasting and the Thyroid State on the Activity of Thyroxine 5′-Monodeiodinase in Rat Liver: A Kinetic Analysis of Microsomal Formation of Triiodothyronine from Thyroxine*
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See all 345

Authors: Docter, R., Krenning, E. P., de Jong, M., & Hennemann, G.
Affiliations: Erasmus MC (NL)
Corresponding author: Docter, R.
ORCID: Krenning, E. P.
Venue: Clinical Endocrinology
Publisher: Wiley
Published: 1993-11
Volume: 39
Issue: 5
Pages: 499-518
ISSN: 0300-0664 (ISSN-L)
1365-2265
DOI: 10.1111/j.1365-2265.1993.tb02401.x
OpenAlex: W2121588417
Cited by: 345
References: 242
Citations by year: 2026: 2 · 2025: 3 · 2024: 4 · 2023: 7 · 2022: 12 · 2021: 6 · 2020: 8 · 2019: 12 · 2018: 6 · 2017: 6 · 2016: 10 · 2015: 10 · 2014: 9 · 2013: 12 · 2012: 10
FWCI: 3.92
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 5250 d)
Locations: Clinical Endocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Cancer Diagnosis and Treatment
Health Sciences › Medicine › Surgery › Thyroid and Parathyroid Surgery
Keywords: low T3 syndrome, thyroid hormones, serum thyroid hormones, thyroid hormone metabolism
MeSH terms: Euthyroid Sick Syndromes, Humans, Thyroid Hormones, Thyrotropin, Thyroxine, Triiodothyronine

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The sick euthyroid syndrome: changes in thyroid hormone serum parameters and hormone metabolism

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