Serum leptin, thyroxine and thyroid-stimulating hormone levels interact to affect cognitive function among US adults: Evidence from a large representative survey

Neurobiology of Aging

Volumn 33, Issue 8, 2012, Pages 1730-1743

  Beydoun, May A ^a   Beydoun, Hind A ^b   Shroff, Monal R ^c   Kitner Triolo, Melissa H ^a   Zonderman, Alan B ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Aging; Cognitive function; Leptin; Thyroid stimulating hormone; Thyroxine

Indexed keywords

LEPTIN; THYROTROPIN; THYROXINE;

ADULT; AGED; ARTICLE; COGNITION; CONTROLLED STUDY; FEMALE; HEALTH SURVEY; HORMONE BLOOD LEVEL; HUMAN; LEPTIN BLOOD LEVEL; MALE; MATHEMATICS; NEUROPSYCHOLOGICAL TEST; PERFORMANCE; PRIORITY JOURNAL; RECALL; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; UNITED STATES;

ADULT; AGE DISTRIBUTION; AGED; AGED, 80 AND OVER; AGING; BIOLOGICAL MARKERS; COGNITION; COGNITION DISORDERS; EVIDENCE-BASED MEDICINE; FEMALE; HEALTH SURVEYS; HUMANS; LEPTIN; MALE; MIDDLE AGED; PREVALENCE; THYROTROPIN; THYROXINE; UNITED STATES; YOUNG ADULT;

EID: 84861871532     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.05.008     Document Type: Article

References (66)

1. Almeida C., Vaisman M., Costa A.J., Reis F.A., Reuters V., Teixeira P., Ferreira M., Teixeira L.B., Araujo G.R., Brasil M.A. Are neuropsychological changes relevant in subclinical hypothyroidism?. Arq. Bras. Endocrinol. Metab 2007, 51:606-611.
2. Anderson G.W. Thyroid hormones and the brain. Front. Neuroendocrinol 2001, 22:1-17.
3. Bauer M., Whybrow P.C. Thyroid hormone, neural tissue and mood modulation. World J. Biol. Psychiatry 2001, 2:59-69.
4. Belandia B., Latasa M.J., Villa A., Pascual A. Thyroid hormone negatively regulates the transcriptional activity of the beta-amyloid precursor protein gene. J. Biol. Chem 1998, 273:30366-30371.
5. Beydoun M.A., Beydoun H.A., Wang Y. Obesity and central obesity as risk factors for incident dementia and its subtypes: a systematic review and meta-analysis. Obes. Rev 2008, 9:204-218.
6. Biondi B. Thyroid and obesity: an intriguing relationship. J. Clin. Endocrinol. Metab 2010, 95:3614-3617.
7. Bono G., Fancellu R., Blandini F., Santoro G., Mauri M. Cognitive and affective status in mild hypothyroidism and interactions with L-thyroxine treatment. Acta Neurol. Scand 2004, 110:59-66.
8. Burmeister L.A., Ganguli M., Dodge H.H., Toczek T., DeKosky S.T., Nebes R.D. Hypothyroidism and cognition: preliminary evidence for a specific defect in memory. Thyroidology 2001, 11:1177-1185.
9. Canaris G.J., Manowitz N.R., Mayor G., Ridgway E.C. The Colorado thyroid disease prevalence study. Arch. Intern. Med. 2000, 160:526-534.
10. Cárdenas-Ibarra L., Solano-Velázquez J.A., Salinas-Martínez R., Aspera-Ledezma T.D., Sifuentes-Martínez M.del R., Villarreal-Pérez J.Z. Cross-sectional observations of thyroid function in geriatric Mexican outpatients with and without dementia. Arch. Gerontol. Geriatr 2008, 46:173-180.
11. The Third National Health and Nutrition Examination Survey (NHANES III 1988-94) Reference Manuals and Reports (CD-ROM) 1996, Center for Disease Control and Prevention (CDC), Centers for Disease Control and Prevention, Bethesda, MD.
12. Ceresini G., Lauretani F., Maggio M., Ceda G.P., Morganti S., Usberti E., Chezzi C., Valcavi R., Bandinelli S., Guralnik J.M., Cappola A.R., Valenti G., Ferrucci L. Thyroid function abnormalities and cognitive impairment in elderly people: results of the Invecchiare in Chianti study. J. Am. Geriatr. Soc 2009, 57:89-93.
13. Correia N., Mullally S., Cooke G., Tun T.K., Phelan N., Feeney J., Fitzgibbon M., Boran G., O'Mara S., Gibney J. Evidence for a specific defect in hippocampal memory in overt and subclinical hypothyroidism. J. Clin. Endocrinol. Metab 2009, 94:3789-3797.
14. Crantz F.R., Silva J.E., Larsen P.R. An analysis of the sources and quantity of 3,5,3'-triiodothyronine specifically bound to nuclear receptors in rat cerebral cortex and cerebellum. Endocrinology 1982, 110:367-375.
15. de Jong F.J., Masaki K., Chen H., Remaley A.T., Breteler M.M., Petrovitch H., White L.R., Launer L.J. Thyroid function, the risk of dementia and neuropathologic changes: the Honolulu-Asia aging study. Neurobiol. Aging 2009, 30:600-606.
16. Dietrich M.O., Spuch C., Antequera D., Rodal I., de Yébenes J.G., Molina J.A., Bermejo F., Carro E. Megalin mediates the transport of leptin across the blood-CSF barrier. Neurobiol. Aging 2008, 29:902-912.
17. Doherty G.H., Oldreive C., Harvey J. Neuroprotective actions of leptin on central and peripheral neurons in vitro. Neuroscience 2008, 154:1297-1307.
18. Dratman M.B., Crutchfield F.L., Gordon J.T., Jennings A.S. Iodothyronine homeostasis in rat brain during hypo- and hyperthyroidism. Am. J. Physiol 1983, 245:E185-E193.
19. Dugbartey A.T. Neurocognitive aspects of hypothyroidism. Arch. Intern. Med 1998, 158:1413-1418.
20. Evered D.C., Ormston B.J., Smith P.A., Hall R., Bird T. Grades of hypothyroidism. Br. Med. J 1973, 1:657-662.
21. Farooqi I.S., Bullmore E., Keogh J., Gillard J., O'Rahilly S., Fletcher P.C. Leptin regulates striatal regions and human eating behavior. Science 2007, 317:1355.
22. Fewlass D.C., Noboa K., Pi-Sunyer F.X., Johnston J.M., Yan S.D., Tezapsidis N. Obesity-related leptin regulates Alzheimer's Abeta. FASEB J 2004, 18:1870-1878.
23. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res 1975, 12:189-198.
24. Greco S.J., Sarkar S., Johnston J.M., Zhu X., Su B., Casadesus G., Ashford J.W., Smith M.A., Tezapsidis N. Leptin reduces Alzheimer's disease-related tau phosphorylation in neuronal cells. Biochem. Biophys. Res. Commun 2008, 376:536-541.
25. Gunstad J., Spitznagel M.B., Keary T.A., Glickman E., Alexander T., Karrer J., Stanek K., Reese L., Juvancic-Heltzel J. Serum leptin levels are associated with cognitive function in older adults. Brain Res 2008, 1230:233-236.
26. Gunter E.W., Lewis B.G., Koncikowski S.M. Laboratory Procedures Used for the Third National Health and Nutrition Examination Survey (NHANES III), 1988-1994) 2010, US DHHS, Public Health Service, Centers for Disease Control and Prevention, National Center for Environmental Health and National Center for Health Statistics, Atlanta, GA and Hyattsville, MD. http://www.cdc.gov/nchs/data/nhanes/nhanes3/cdrom/nchs/manuals/labman.pdf.
27. Guo Z., Jiang H., Xu X., Duan W., Mattson M.P. Leptin-mediated cell survival signaling in hippocampal neurons mediated by JAK. STAT3 and mitochondrial stabilization. J. Biol. Chem 2008, 283:1754-1763.
28. Gussekloo J., van Exel E., de Craen A.J., Meinders A.E., Frölich M., Westendorp R.G. Thyroid status, disability and cognitive function, and survival in old age. JAMA 2004, 292:2591-2599.
29. Harvey J., Shanley L.J., O'Malley D., Irving A.J. Leptin: a potential cognitive enhancer?. Biochem. Soc. Trans 2005, 33:1029-1032.
30. Harvey J., Solovyova N., Irving A. Leptin and its role in hippocampal synaptic plasticity. Prog. Lipid Res 2006, 45:369-378.
31. Hendrick V., Altshuler L., Whybrow P. Psychoneuroendocrinology of mood disorders. The hypothalamic-pituitary-thyroid axis. Psychiatr. Clin. North Am 1998, 21:277-292.
32. Hogervorst E., Huppert F., Matthews F.E., Brayne C. Thyroid function and cognitive decline in the MRC Cognitive Function and Ageing Study. Psychoneuroendocrinology 2008, 33:1013-1022.
33. Holden K.F., Lindquist K., Tylavsky F.A., Rosano C., Harris T.B., Yaffe K. Serum leptin level and cognition in the elderly: Findings from the Health ABC Study. Neurobiol. Aging 2009, 30:1483-1489. Health ABC Study.
34. Jacob R.J., Dziura J., Medwick M.B., Leone P., Caprio S., During M., Shulman G.I., Sherwin R.S. The effect of leptin is enhanced by microinjection into the ventromedial hypothalamus. Diabetes 1997, 46:150-152.
35. Kramer C.K., von Mühlen D., Kritz-Silverstein D., Barrett-Connor E. Treated hypothyroidism, cognitive function, and depressed mood in old age: the Rancho Bernardo Study. Eur. J. Endocrinol 2009, 161:917-921.
36. Lieb W., Beiser A.S., Vasan R.S., Tan Z.S., Au R., Harris T.B., Roubenoff R., Auerbach S., DeCarli C., Wolf P.A., Seshadri S. Association of plasma leptin levels with incident Alzheimer disease and MRI measures of brain aging. JAMA 2009, 302:2565-2572.
37. Lisi S., Segnani C., Mattii L., Botta R., Marcocci C., Dolfi A., McCluskey R.T., Pinchera A., Bernardini N., Marinò M. Thyroid dysfunction in megalin deficient mice. Mol. Cell. Endocrinol 2005, 236:43-47.
38. Loosen P.T. Effects of thyroid hormones on central nervous system in aging. Psychoneuroendocrinology 1992, 17:355-374.
39. Mafrica F., Fodale V. Thyroid function, Alzheimer's disease and postoperative cognitive dysfunction: a tale of dangerous liaisons?. J. Alzheimers Dis 2008, 14:95-105.
40. Mariotti S., Franceschi C., Cossarizza A., Pinchera A. The aging thyroid. Endocr. Rev 1995, 16:686-715.
41. McCullough M.L., Feskanich D., Rimm E.B., Giovannucci E.L., Ascherio A., Variyam J.N., Spiegelman D., Stampfer M.J., Willett W.C. Adherence to the Dietary Guidelines for Americans and risk of major chronic disease in men. Am. J. Clin. Nutr 2000, 72:1223-1231.
42. McDermott M.T., Ridgway E.C. Subclinical hypothyroidism is mild thyroid failure and should be treated. J. Clin. Endocrinol. Metab 2001, 86:4585-4590.
43. Miller K.J., Parsons T.D., Whybrow P.C., van Herle K., Rasgon N., van Herle A., Martinez D., Silverman D.H., Bauer M. Memory improvement with treatment of hypothyroidism. Int. J. Neurosci 2006, 116:895-906.
44. Monzani F., Del Guerra P., Caraccio N., Pruneti C.A., Pucci E., Luisi M., Baschieri L. Subclinical hypothyroidism: neurobehavioral features and beneficial effect of L-thyroxine treatment. Clin. Investig 1993, 71:367-371.
45. Morrison C.D. Leptin signaling in brain: A link between nutrition and cognition?. Biochim. Biophys. Acta 2009, 1792:401-408.
46. Osterweil D., Syndulko K., Cohen S.N., Pettler-Jennings P.D., Hershman J.M., Cummings J.L., Tourtellotte W.W., Solomon D.H. Cognitive function in non-demented older adults with hypothyroidism. J. Am. Geriatr. Soc 1992, 40:325-335.
47. Paz-Filho G.J., Babikian T., Asarnow R., Delibasi T., Esposito K., Erol H.K., Wong M.L., Licinio J. Leptin replacement improves cognitive development. PLoS One 2008, 3:e3098.
48. Prinz P.N., Scanlan J.M., Vitaliano P.P., Moe K.E., Borson S., Toivola B., Merriam G.R., Larsen L.H., Reed H.L. Thyroid hormones: positive relationships with cognition in healthy, euthyroid older men. J. Gerontol. A Biol. Sci. Med. Sci 1999, 54:M111-M116.
49. Robbins J. Thyroid hormone transport proteins and the physiology of hormone binding. The Thyroid: A Fundamental and Clinical Text 1996, 96-111. Lippincott-Raven, Philadelphia. L.E. Braverman, R.D. Utiger (Eds.).
50. Samuels M.H., Schuff K.G., Carlson N.E., Carello P., Janowsky J.S. Health status, mood, and cognition in experimentally induced subclinical hypothyroidism. J. Clin. Endocrinol. Metab 2007, 92:2545-2551.
51. Samuels M.H., Schuff K.G., Carlson N.E., Carello P., Janowsky J.S. Health status, psychological symptoms, mood, and cognition in L-thyroxine-treated hypothyroid subjects. Thyroidology 2007, 17:249-258.
52. Selvin S. Statistical Analysis of Epidemiologic Data 2004, Oxford University Press, New York, NY. third ed.
53. Shanley L.J., Irving A.J., Harvey J. Leptin enhances NMDA receptor function and modulates hippocampal synaptic plasticity. J. Neurosci. 2001, 21:RC186.
54. Smith J.W., Evans A.T., Costall B., Smythe J.W. Thyroid hormones, brain function and cognition: a brief review. Neurosci. Biobehav. Rev 2002, 26:45-60.
55. Statistics/Data Analysis 2009, STATA, Release 11, 0, Stata Corporation, College Station, TX.
56. Stern R.A., Davis J.D., Rogers B.L., Smith K.E., Harrington C.J., Ott B.R., Jackson I.M., Prange A.J. Preliminary study of the relationship between thyroid status and cognitive and neuropsychiatric functioning in euthyroid patients with Alzheimer dementia. Cogn. Behav. Neurol 2004, 17:219-223.
57. Stuerenburg H.J., Arlt S., Mueller-Thomsen T. Free thyroxine, cognitive decline and depression in Alzheimer's disease. Neuro Endocrinol. Lett 2006, 27:535-537.
58. Surks M.I., Chopra I.J., Mariash C.N., Nicoloff J.T., Solomon D.H. American Thyroid Association guidelines for use of laboratory tests in thyroid disorders. JAMA 1990, 263:1529-1532.
59. Tezapsidis N., Johnston J.M., Smith M.A., Ashford J.W., Casadesus G., Robakis N.K., Wolozin B., Perry G., Zhu X., Greco S.J., Sarkar S. Leptin: a novel therapeutic strategy for Alzheimer's disease. J. Alzheimers Dis 2009, 16:731-740.
60. Documentation on leptin assay. The Third National Health and Nutrition Examination Survey (NHANES III), 1988-94, Series 11, No. 12A (Serum Leptin Data and Documentation) Data Release 2002, US DHHS, PHS, Centers for Disease Control and Prevention, National Center for Environmental Health and National Center for Health Statistics, Atlanta, GA and Hyattsville, MD. http://ftp://ftp.cdc.gov/pub/Health_Statistics/NCHS/nhanes/nhanes3/12A/le-acc.pdf.
61. Volpato S., Guralnik J.M., Fried L.P., Remaley A.T., Cappola A.R., Launer L.J. Serum thyroxine level and cognitive decline in euthyroid older women. Neurology 2002, 58:1055-1061.
62. Wahlin A., Wahlin T.B., Small B.J., Backman L. Influences of thyroid stimulating hormone on cognitive functioning in very old age. J. Gerontol. B Psychol. Sci. Soc. Sci 1998, 53:234-239.
63. Weng Z., Signore A.P., Gao Y., Wang S., Zhang F., Hastings T., Yin X.M., Chen J. Leptin protects against 6-hydroxydopamine-induced dopaminergic cell death via mitogen-activated protein kinase signaling. J. Biol. Chem 2007, 282:34479-34491.
64. Wu T., Flowers J.W., Tudiver F., Wilson J.L., Punyasavatsut N. Subclinical thyroid disorders and cognitive performance among adolescents in the United States. BMC Pediatr 2006, 6:12.
65. Zhang F., Wang S., Signore A.P., Chen J. Neuroprotective effects of leptin against ischemic injury induced by oxygen-glucose deprivation and transient cerebral ischemia. Stroke 2007, 38:2329-2336.
66. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372:425-432.