Hypothyroxinemia of prematurity: Cause, diagnosis and management

Expert Review of Endocrinology and Metabolism

Volumn 3, Issue 4, 2008, Pages 453-462

  May Ng, Sze ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Hypothyroxinemia; Prematurity; Thyroid hormonies; Thyroxine T4

Indexed keywords

IODINE; LIOTHYRONINE; MONOCARBOXYLATE TRANSPORTER 8; PLACEBO; RETINOID X RECEPTOR; THYROID HORMONE; THYROXINE;

BIOSYNTHESIS; BRAIN DAMAGE; BRAIN DEVELOPMENT; CELL MIGRATION; CLINICAL TRIAL; COGNITIVE DEFECT; CONGENITAL HYPOTHYROIDISM; DISEASE ASSOCIATION; DRUG EFFICACY; EMBRYO DEVELOPMENT; HORMONAL THERAPY; HORMONE METABOLISM; HORMONE SUBSTITUTION; HORMONE TRANSPORT; HUMAN; HYPERTENSION; HYPERTHYROIDISM; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INCIDENCE; INTELLIGENCE QUOTIENT; IODINE DEFICIENCY; LOW BIRTH WEIGHT; NERVOUSNESS; NEWBORN DISEASE; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PREMATURITY; PRIORITY JOURNAL; RESPIRATORY DISTRESS SYNDROME; REVIEW; RISK FACTOR; RISK REDUCTION; SIDE EFFECT; TACHYCARDIA; THYROID FUNCTION; THYROID HORMONE BLOOD LEVEL; VISUOMOTOR COORDINATION; VITAMIN SUPPLEMENTATION; WEIGHT REDUCTION;

EID: 55749103039     PISSN: 17446651     EISSN: None     Source Type: Journal    
DOI: 10.1586/17446651.3.4.453     Document Type: Review

References (100)

1. Bernal J. Thyroid hormones and brain development. Vitam. Horm. 71, 95-122 (2005).
2. Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Role of thyroid hormone during early brain development. Eur. J. Endocrinol. 151(Suppl. 3), U25-U37 (2004).
3. Fisher DA, Klein AH. Thyroid development and disorders of thyroid function in the newborn. N. Engl. J. Med. 304(12), 702-712 (1981).
4. LaFranchi SH, Haddow JE, Hollowell JG. Is thyroid inadequacy during gestation a risk factor for adverse pregnancy and developmental outcomes? Thyroid 15(1), 60-71 (2005).
5. Williams FL, Simpson J, Delahunty C et al. Developmental trends in cord and postpartum serum thyroid hormones in preterm infants. J. Clin. Endocrinol. Metab. 89(11), 5314-5320 (2004).
6. LaFranchi S. Thyroid function in the preterm infant. Thyroid 9(1), 71-78 (1999).
7. La Gamma EF, van Wassenaer AG, Golombek SG et al. Neonatal thyroxine supplementation for transient hypothyroxinemia of prematurity: beneficial or detrimental? Treat. Endocrinol. 5(6), 335-346 (2006).
8. Williams FL, Visser TJ, Hume R. Transient hypothyroxinaemia in preterm infants. Early Hum. Dev. 82(12), 797-802 (2006).
9. van Wassenaer AG, Kok JH, Dekker FW, de Vijlder JJ. Thyroid function in very preterm infants: influences of gestational age and disease. Pediatr. Res. 42(5), 604-609 (1997).
10. Salerno M, Militerni R, Di Maio S, Bravaccio C, Gasparini N, Tenore A. Intellectual outcome at 12 years of age in congenital hypothyroidism. Eur. J. Endocrinol. 141(2), 105-110 (1999).
11. Song SI, Daneman D, Rovet J. The influence of etiology and treatment factors on intellectual outcome in congenital hypothyroidism. J. Dev. Behav. Pediatr. 22(6), 376-384 (2001).
12. Wood NS, Costeloe K, Gibson AT, Hennessy EM, Marlow N, Wilkinson AR. The EPICure study: associations and antecedents of neurological and developmental disability at 30 months of age following extremely preterm birth. Arch. Dis. Child. Fetal Neonatal Ed. 90(2), F134-F140 (2005).
13. Marlow N, Wolke D, Bracewell MA, Samara M. Neurologic and developmental disability at six years of age after extremely preterm birth. N. Engl. J. Med. 352(1), 9-19 (2005).
14. Vohr BR, Allen M. Extreme prematurity - the continuing dilemma. N. Engl. J. Med. 352(1), 71-72 (2005).
15. Obregon MJ, Calvo EM, Del Rey FE, de Escobar GM. Ontogenesis of thyroid function and interactions with maternal function. Endocr. Dev. 10, 86-98 (2007).
16. Evans TC, Kretzschmar RM, Hodges RE, Song CW. Radioiodine uptake studies of the human fetal thyroid. J. Nucl. Med. 8(3), 157-165 (1967).
17. Beierwaltes WH, Crane HR, Wegst A, Spafford NR, Carr EA Jr. Radioactive iodine concentration in the fetal human thyroid gland from fall-out. JAMA 173, 1895-1902 (1960).
18. Davies A, Blakeney AGH, Kidd C. Human Physiology. Churchill Livingstone, Oxford, UK (2004).
19. Kester MH, Martinez de Mena R, Obregon MJ et al. Iodothyronine levels in the human developing brain: major regulatory roles of iodothyronine deiodinases in different areas. J. Clin. Endocrinol. Metab. 89(7), 3117-3128 (2004).
20. Bernal J. Thyroid hormone receptors in brain development and function. Nat. Clin. Pract. Endocrinol. Metab. 3(3), 249-259 (2007).
21. Yen PM, Ando S, Feng X, Liu Y, Maruvada P, Xia X. Thyroid hormone action at the cellular, genomic and target gene levels. Mol. Cell. Endocrinol. 246(1-2), 121-127 (2006).
22. Iskaros J, Pickard M, Evans I, Sinha A, Hardiman P, Ekins R. Thyroid hormone receptor gene expression in first trimester human fetal brain. J. Clin. Endocrinol. Metab. 85(7), 2620-2623 (2000).
23. Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J. Clin. Endocrinol. Metab. 85(11), 3975-3987 (2000).
24. Bernal J, Pekonen F. Ontogenesis of the nuclear 3,5,3′-triiodothyronine receptor in the human fetal brain. Endocrinology 114(2), 677-679 (1984).
25. Berbel P, Guadano-Ferraz A, Angulo A, Ramon Cerezo J. Role of thyroid hormones in the maturation of interhemispheric connections in rats. Behav. Brain Res. 64(1-2), 9-14 (1994).
26. Lavado-Autric R, Auso E, Garcia-Velasco JV et al. Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J. Clin. Invest. 111(7), 1073-1082 (2003).
27. Vulsma T, Gons MH, de Vijlder JJ. Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. N. Engl. J. Med. 321(1), 13-16 (1989).
28. Chowdhry P, Scanlon JW, Auerbach R, Abbassi V. Results of controlled double-blind study of thyroid replacement in very low-birth-weight premature infants with hypothyroxinemia. Pediatrics 73(3), 301-305 (1984).
29. Biswas S, Buffery J, Enoch H, Bland JM, Walters D, Markiewicz M. A longitudinal assessment of thyroid hormone concentrations in preterm infants younger than 30 weeks' gestation during the first 2 weeks of life and their relationship to outcome. Pediatrics 109(2), 222-227 (2002).
30. Uhrmann S, Marks KH, Maisels MJ et al. Thyroid function in the preterm infant: a longitudinal assessment. J. Pediatr. 92(6), 968-973 (1978).
31. Diamond FB, Parks JS, Tenore A, Marino JM, Bongiovanni AM. Hypothyroxinemia in sick and well preterm infants. Clin. Pediatr. (Phila.) 18(9), 555, 559-561 (1979).
32. Costa A, Arisio R, Benedetto C et al. Thyroid hormones in tissues from human embryos and fetuses. J. Endocrinol. Invest. 14(7), 559-568 (1991).
33. James SR, Franklyn JA, Kilby MD. Placental transport of thyroid hormone. Best Pract. Res. Clin. Endocrinol. Metab. 21(2), 253-264 (2007).
34. de Escobar GM, Obregon MJ, del Rey FE. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract. Res. Clin. Endocrinol. Metab. 18(2), 225-248 (2004).
35. van den Hove MF, Beckers C, Devlieger H, de Zegher F, De Nayer P. Hormone synthesis and storage in the thyroid of human preterm and term newborns: effect of thyroxine treatment. Biochimie 81(5), 563-570 (1999).
36. Ibrahim M, de Escobar GM, Visser TJ et al. Iodine deficiency associated with parenteral nutrition in extreme preterm infants. Arch. Dis. Child. Fetal Neonatal Ed. 88(1), F56-F57 (2003).
37. Rogahn J, Ryan S, Wells J et al. Randomised trial of iodine intake and thyroid status in preterm infants. Arch. Dis. Child. Fetal Neonatal Ed. 83(2), F86-F90 (2000).
38. van Wassenaer AG, Stulp MR, Valianpour F et al. The quantity of thyroid hormone in human milk is too low to influence plasma thyroid hormone levels in the very preterm infant. Clin. Endocrinol. (Oxf.) 56(5), 621-627 (2002).
39. Murphy N, Hume R, van Toor H et al. The hypothalamic-pituitary-thyroid axis in preterm infants; changes in the first 24 hours of postnatal life. J. Clin. Endocrinol. Metab. 89(6), 2824-2831 (2004).
40. Biswas S, Buffery J, Enoch H, Bland M, Markiewicz M, Walters D. Pulmonary effects of triiodothyronine (T3) and hydrocortisone (HG) supplementation in preterm infants less than 30 weeks gestation: results of the THORN trial - thyroid hormone replacement in neonates. Pediatr. Res. 53(1), 48-56 (2003).
41. Ng PC, Lee CH, Lam CW et al. Transient adrenocortical insufficiency of prematurity and systemic hypotension in very low birthweight infants. Arch. Dis. Child. Fetal Neonatal Ed. 89(2), F119-F126 (2004).
42. Scott SM, Cimino DF. Evidence for developmental hypopituitarism in ill preterm infants. J. Perinatol. 24(7), 429-434 (2004).
43. Watterberg KL. Adrenocortical function and dysfunction in the fetus and neonate. Semin. Neonatal. 9(1), 13-21 (2004).
44. Watterberg KL, Gerdes JS, Cole CH et al. Prophylaxis of early adrenal insufficiency to prevent bronchopulmonary dysplasia: a multicenter trial. Pediatrics 114(6), 1649-1657 (2004).
45. Valerio PG, van Wassenaer AG, de Vijlder JJ, Kok JH. A randomized, masked study of triiodothyronine plus thyroxine administration in preterm infants less than 28 weeks of gestational age: hormonal and clinical effects. Pediatr. Res. 55(2), 248-253 (2004).
46. Tohei A, Imai A, Watanabe G, Taya K. Influence of thiouracil-induced hypothyroidism on adrenal and gonadal functions in adult female rats. J. Vet. Med. Sci. 60(4), 439-446 (1998).
47. Klein RZ, Carlton EL, Faix JD et al. Thyroid function in very low birth weight infants. Clin. Endocrinol. (Oxf.) 47(4), 411-417 (1997).
48. Fisher DA. Euthyroid low thyroxine (T4) and triiodothyronine (T3) states in prematures and sick neonates. Pediatr. Clin. North Am. 37(6), 1297-1312 (1990).
49. Yeung MY, Smyth JP. Hormonal factors in the morbidities associated with extreme prematurity and the potential benefits of hormonal supplement. Biol. Neonate 81(1), 1-15 (2002).
50. DeGroot LJ. "Non-thyroidal illness syndrome" is functional central hypothyroidism, and if severe, hormone replacement is appropriate in light of present knowledge. J. Endocrinol. Invest. 26(12), 1163-1170 (2003).
51. Adler SM, Wartofsky L. The nonthyroidal illness syndrome. Endocrinol. Metab. Clin. North Am. 36(3), 657-672, vi (2007).
52. Inder TE, Warfield SK, Wang H, Huppi PS, Volpe JJ. Abnormal cerebral structure is present at term in premature infants. Pediatrics 115(2), 286-294 (2005).
53. Huppi PS, Warfield S, Kikinis R et al. Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann. Neurol. 43(2), 224-235 (1998).
54. Bourgeois JP. Synaptogenesis, heterochrony and epigenesis in the mammalian neocortex. Acta Paediatr. 422(Suppl.), 27-33 (1997).
55. Cooke RW. Preterm mortality and morbidity over 25 years. Arch. Dis. Child. Fetal Neonatal Ed. 91(4), F293-F294 (2006).
56. Abernethy LJ, Cooke RW, Foulder-Hughes L. Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm. Pediatr. Res. 55(5), 884-893 (2004).
57. Peterson BS, Vohr B, Staib LH et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 284(15), 1939-1947 (2000).
58. Cooke RW. Are there critical periods for brain growth in children born preterm? Arch. Dis. Child. Fetal Neonatal Ed. 91(1), F17-F20 (2006).
59. Abernethy LJ, Klaflowski G, Foulder-Hughes L, Cooke RW. Magnetic resonance imaging and T2 relaxometry of cerebral white matter and hippocampus in children born preterm. Pediatr: Res. 54(6), 868-874 (2003).
60. Inder TE, Huppi PS, Warfield S et al. Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term. Ann. Neurol. 46(5), 755-760 (1999).
61. Salerno M, Militerni R, Bravaccio C et al. Effect of different starting doses of levothyroxine on growth and intellectual outcome at four years of age in congenital hypothyroidism. Thyroid 12(1), 45-52 (2002).
62. Rovet JE, Hepworth S. Attention problems in adolescents with congenital hypothyroidism: a multicomponential analysis. J. Int. Neuropsychol. Soc. 7(6), 734-744 (2001).
63. Ishaik G, Asztalos E, Perlman K, Newton S, Frisk V, Rovet J. Hypothyroxinemia of prematurity and infant neurodevelopment: a pilot study. J. Dev. Behav. Pediatr. 21(3), 172-179 (2000).
64. Anderson GW. Thyroid hormone and cerebellar development. Cerebellum (2008).
65. Gupta RK, Bhatia V, Poptani H, Gujral RB. Brain metabolite changes on in vivo proton magnetic resonance spectroscopy in children with congenital hypothyroidism. J. Pediatr. 126(3), 389-392 (1995).
66. Jagannathan NR, Tandon N, Raghunathan P, Kochupillai N. Reversal of abnormalities of myelination by thyroxine therapy in congenital hypothyroidism: localized in vivo proton magnetic resonance spectroscopy (MRS) study. Brain Res. Dev. Brain Res. 109(2), 179-186 (1998).
67. Crisanti P, Omri B, Hughes EJ et al. The expression of thyrotropin receptors in the brain. Endocrinology 142, 812-822 (2001).
68. Schoonover CM, Seibel MM, Jolson DM et al. Thyroid hormone regulates oligodendrocyte accumulation in developing rat brain white matter tracts. Endocrinology 145(11), 5013-5020 (2004).
69. Jones SA, Jolson DM, Cuta KK, Mariash CN, Anderson GW. Triiodothyronine is a survival factor for developing oligodendrocytes. Mol. Cell. Endocrinol. 199(1-2), 49-60 (2003).
70. Schwartz CE, Stevenson RE. The MCT8 thyroid hormone transporter and Allan-Herndon-Dudley syndrome. Best Pract. Res. Clin. Endocrinol. Metab. 21(2), 307-321 (2007).
71. Schwartz CE, May MM, Carpenter NJ et al. Allan-Herndon-Dudley syndrome and the monocarboxylate transporter 8 (MCT8) gene. Am.J. Hum. Genet. 77(1), 41-53 (2005).
72. Cai D, Su Q, Chen Y, Luo M. Effect of thyroid hormone deficiency on developmental expression of goalpha gene in the brain of neonatal rats by competitive RT-PCR and in situ hybridization histochemistry. Brain Res. 864(2), 195-204 (2000).
73. Iniguez MA, De Lecea L, Guadano-Ferraz A et al. Cell-specific effects of thyroid hormone on RC3/neurogranin expression in rat brain. Endocrinology 137(3), 1032-1041 (1996).
74. Auso E, Lavado-Autric R, Cuevas E, Del Rey FE, Morreale De Escobar G, Berbel P. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migraion. Endocrinology 145(9), 4037-4047 (2004).
75. Eayrs JT, Horn G. The development of cerebral cortex in hypothyroid and starved rats. Anat. Rec. 121(1), 53-61 (1955).
76. Eayrs JT. Thyroid hypofunction and the development of the central nervous system. Nature 172(4374), 403-404 (1953).
77. Berbel P, Auso E, Garcia-Velasco JV, Molina ML, Camacho M. Role of thyroid hormones in the maturation and organisation of rat barrel cortex. Neuroscience 107(3), 383-394 (2001).
78. Nicholson JL, Altman J. The effects of early hypo- and hyperthyroidism on the development of the rat cerebellar cortex. II. Synaptogenesis in the molecular layer. Brain Res. 44(1), 25-36 (1972).
79. Xiao Q, Nikodem VM. Apoptosis in the developing cerebellum of the thyroid hormone deficient rat. Front. Biosci. 3, A52-A57 (1998).
80. Balazs R, Kovacs S, Cocks WA, Johnson AL, Eayrs JT. Effect of thyroid hormone on the biochemical maturation of rat brain: postnatal cell formation. Brain Res. 25(3), 555-570 (1971).
81. Balazs R, Brooksbank BW, Davison AN, Eayrs JT, Wilson DA. The effect of neonatal thyroidectomy on myelination in the rat brain. Brain Res. 15(1), 219-232 (1969).
82. Reuss ML, Paneth N, Pinto-Martin JA, Lorenz JM, Susser M. The relation of transient hypothyroxinemia in preterm infants to neurologic development at two years of age. N. Engl. J. Med. 334(13), 821-827 (1996).
83. Den Ouden AL, Kok JH, Verkerk PH, Brand R, Verloove-Vanhorick SP. The relation between neonatal thyroxine levels and neurodevelopmental outcome at age 5 and 9 years in a national cohort of very preterm and/or very low birth weight infants. Pediatr. Res. 39(1), 142-145 (1996).
84. Leviton A, Paneth N, Reuss ML et al. Hypothyroxinemia of prematurity and the risk of cerebral white matter damage. J. Pediatr. 134(6), 706-711 (1999).
85. Paul DA, Leef KH, Stefano JL, Bartoshesky L. Low serum thyroxine on initial newborn screening is associated with intraventricular hemorrhage and death in very low birth weight infants. Pediatrics 101(5), 903-907 (1998).
86. Lucas A, Morley R, Fewtrell MS. Low triiodothyronine concentration in preterm infants and subsequent intelligence quotient (IQ) at 8 year follow up. BMJ 312(7039), 1132-1133 (1996).
87. Meijer WJ, Verloove-Vanhorick SP, Brand R, van den Brande JL. Transient hypothyroxinaemia associated with developmental delay in very preterm infants. Arch. Dis. Child. 67(7), 944-947 (1992).
88. Osborn D, Hunt R. Prophylactic postnatal thyroid hormones for prevention of morbidity and mortality in preterm infants. Cochrane Database Syst. Rev. 1, CD005948 (2007).
89. Vanhole C, Aerssens P, Naulaers G et al. L-thyroxine treatment of preterm newborns: clinical and endocrine effects. Pediatr. Res. 42(1), 87-92 (1997).
90. van Wassenaer AG, Kok JH, de Vijlder JJ et al. Effects of thyroxine supplementation on neurologic development in infants born at less than 30 weeks' gestation. N. Engl. J. Med. 336(1), 21-26 (1997).
91. van Wassenaer AG, Westera J, Houtzager BA, Kok JH. Ten year follow up of children born at < 30 weeks' gestational age supplemented with thyroxine in the neonatal period in a randomized controlled trial. Pediatrics 116(5), e613-e618 (2005).
92. Smith LM, Leake RD, Berman N, Villanueva S, Brasel JA. Postnatal thyroxine supplementation in infants less than 32 weeks' gestation: effects on pulmonary morbidity. J. Perinatol. 20(7), 427-431 (2000).
93. Kodding R, Fuhrmann H, von zur Muhlen A. Investigations on iodothyronine deiodinase activity in the maturing rat brain. Endocrinology 118(4), 1347-1352 (1986).
94. Calvo R, Obregon MJ, Ruiz de Ona C, Escobar del Rey F, Morreale de Escobar G. Congenital hypothyroidism, as studied in rats. Crucial role of maternal thyroxine but not of 3,5,3′-triiodothyronine in the protection of the fetal brain. J. Clin. Invest. 86(3), 889-899 (1990).
95. van Wassenaer AG, Kok JH, Dekker FW, Endert E, de Vijlder JJ. Thyroxine administration to infants of less than 30 weeks gestational age decreases plasma tri-iodothyronine concentrations. Eur. J. Endocrinol. 139(5), 508-515 (1998).
96. van Wassenaer AG, Briet JM, van Baar A et al. Free thyroxine levels during the first weeks of life and neurodevelopmental outcome until the age of 5 years in very preterm infants. Pediatrics 110(3), 534-539 (2002).
97. Lucas A, Rennie J, Baker BA, Morley R. Low plasma triiodothyronine concentrations and outcome in preterm infants. Arch. Dis. Child. 63(10), 1201-1206 (1988).
98. Thienpont LM, Beastall G, Christofides ND et al. Proposal of a candidate international conventional reference measurement procedure for free thyroxine in serum. Clin. Chem. Lab. Med. 45(7), 934-936 (2007).
99. Holm SS, Hansen SH, Faber J, Staun-Olsen P. Reference methods for the measurement of free thyroid hormones in blood: evaluation of potential reference methods for free thyroxine. Clin. Biochem. 37(2), 85-93 (2004).
100. Deming DD, Rabin CW, Hopper AO, Peverini RL, Vyhmeister NR, Nelson JC. Direct equilibrium dialysis compared with two non-dialysis free T4 methods in premature infants. J. Pediatr. 151(4), 404-408 (2007).