Cushing's syndrome causes irreversible effects on the human brain: A systematic review of structural and functional magnetic resonance imaging studies

European Journal of Endocrinology

Volumn 173, Issue 1, 2015, Pages R1-R14

  Andela, Cornelie D ^a,b   Van Haalen, Femke M ^a   Ragnarsson, Oskar ^c   Papakokkinou, Eleni ^c   Johannsson, Gudmundur ^c   Santos, Alicia ^d   Webb, Susan M ^d   Biermasz, Nienke R ^a,b   Van Der Wee, Nic J A ^a,b   Pereira, Alberto M ^a,b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^d UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; HYDROCORTISONE; TRIACYLGLYCEROL;

ACTIVE DISEASE; AGE; BEHAVIOR; BRAIN ATROPHY; BRAIN BIOCHEMISTRY; BRAIN DISEASE; BRAIN FUNCTION; BRAIN LEVEL; BRAIN SIZE; BRAIN VENTRICLE DILATATION; CLINICAL FEATURE; COGNITION; CUSHING SYNDROME; DISEASE ASSOCIATION; DISEASE DURATION; EMOTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENERAL ASPECTS OF DISEASE; GRAY MATTER; HIPPOCAMPAL VOLUME; HUMAN; HYPERCORTISOLISM; LONGITUDINAL STUDY; MENTAL DISEASE; MOOD; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUALITY OF LIFE; REMISSION; REVIEW; STRUCTURAL MAGNETIC RESONANCE IMAGING; SYSTEMATIC REVIEW; BRAIN; COMPLICATION; CONVALESCENCE; META ANALYSIS; PATHOLOGY;

BRAIN; CUSHING SYNDROME; HUMANS; MAGNETIC RESONANCE IMAGING; RECOVERY OF FUNCTION;

EID: 84935084892     PISSN: 08044643     EISSN: 1479683X     Source Type: Journal    
DOI: 10.1530/EJE-14-1101     Document Type: Review

References (51)

1. Carroll TB, Aron DC, Findling JW & Tyrrell JB. Glucocorticoids and Adrenal Androgens. In Basic and clinical endocrinology, edn 9, ch. 9, pp 317-318. Eds Gardner D & Shoback D. Singapore: McGrawHill, 2011.
2. Newell-Price J, Bertagna X, Grossman AB & Nieman LK. Cushing's syndrome. Lancet 2006 367 1605-1617. (doi:10.1016/S0140-6736(06)68699-6)
3. Colao A, Pivonello R, Spiezia S, Faggiano A, Ferone D, Filippella M, Marzullo P, Cerbone G, Siciliani M & Lombardi G. Persistence of increased cardiovascular risk in patients with Cushing's disease after five years of successful cure. Journal of Clinical Endocrinology and Metabolism 1999 84 2664-2672. (doi:10.1210/jcem.84.8.5896)
4. Dekkers OM, Biermasz NR, Pereira AM, Roelfsema F, van Aken MO, Voormolen JH & Romijn JA. Mortality in patients treated for Cushing's disease is increased, compared with patients treated for nonfunctioning pituitary macroadenoma. Journal of Clinical Endocrinology and Metabolism 2007 92 976-981. (doi:10.1210/jc.2006-2112)
5. Dekkers OM, Horvath-Puho E, Jorgensen JO, Cannegieter SC, Ehrenstein V, Vandenbroucke JP, Pereira AM & Sorensen HT. Multisystem morbidity and mortality in Cushing's syndrome: a cohort study. Journal of Clinical Endocrinology and Metabolism 2013 98 2277-2284. (doi:10.1210/jc.2012-3582)
6. van Aken MO, Pereira AM, Biermasz NR, van Thiel SW, Hoftijzer HC, Smit JW, Roelfsema F, Lamberts SW & Romijn JA. Quality of life in patients after long-term biochemical cure of Cushing's disease. Journal of Clinical Endocrinology and Metabolism 2005 90 3279-3286. (doi:10.1210/jc.2004-1375)
7. Tiemensma J, Kokshoorn NE, Biermasz NR, Keijser BJ, Wassenaar MJ, Middelkoop HA, Pereira AM & Romijn JA. Subtle cognitive impairments in patients with long-term cure of Cushing's disease. Journal of Clinical Endocrinology and Metabolism 2010 95 2699-2714. (doi:10.1210/jc.2009-2032)
8. Peace KA, Orme SM, Thompson AR, Padayatty S, Ellis AW &Belchetz PE. Cognitive dysfunction in patients treated for pituitary tumours. Journal of Clinical and Experimental Neuropsychology 1997 19 1-6. (doi:10.1080/01688639708403831)
9. Trethowan WH & Cobb S. Neuropsychiatric aspects of Cushing's syndrome. A.M.A. Archives of Neurology and Psychiatry 1952 67 283-309. (doi:10.1001/archneurpsyc.1952.02320150016002)
10. Momose KJ, Kjellberg RN & Kliman B. High incidence of cortical atrophy of the cerebral and cerebellar hemispheres in Cushing's disease. Radiology 1971 99 341-348. (doi:10.1148/99.2.341)
11. Starkman MN, Gebarski SS, Berent S & Schteingart DE. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biological Psychiatry 1992 32 756-765. (doi:10.1016/0006-3223(92)90079-F)
12. Starkman MN, Giordani B, Gebarski SS, Berent S, Schork MA &Schteingart DE. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biological Psychiatry 1999 46 1595-1602. (doi:10.1016/S0006-3223(99)00203-6)
13. Starkman MN, Giordani B, Gebarski SS & Schteingart DE. Improvement in learning associated with increase in hippocampal formation volume. Biological Psychiatry 2003 53 233-238. (doi:10.1016/S0006-3223(02)01750-X)
14. Seixas D, Foley P, Palace J, Lima D, Ramos I & Tracey I. Pain in multiple sclerosis: a systematic review of neuroimaging studies. NeuroImage. Clinical 2014 5 322-331. (doi:10.1016/j.nicl.2014.06.014)
15. Bourdeau I, Bard C, Noel B, Leclerc I, Cordeau MP, Belair M, Lesage J, Lafontaine L & Lacroix A. Loss of brain volume in endogenous Cushing's syndrome and its reversibility after correction of hypercortisolism. Journal of Clinical Endocrinology and Metabolism 2002 87 1949-1954. (doi:10.1210/jcem.87.5.8493)
16. Crespo I, Granell-Moreno E, Santos A, Valassi E, Vives-Gilabert Y, de Juan-Delago M, Webb SM, Gomez-Anson B & Resmini E. Impaired decision-making and selective cortical frontal thinning in Cushing's syndrome. Clinical Endocrinology 2014 81 826-833. (doi:10.1111/cen.12564)
17. Resmini E, Santos A, Gomez-Anson B, Vives Y, Pires P, Crespo I, Portella MJ, de Juan-Delago M, Barahona MJ & Webb SM. Verbal and visual memory performance and hippocampal volumes, measured by 3-Tesla magnetic resonance imaging, in patients with Cushing's syndrome. Journal of Clinical Endocrinology and Metabolism 2012 97 663-671. (doi:10.1210/jc.2011-2231)
18. Resmini E, Santos A, Gomez-Anson B, Lopez-Mourelo O, Pires P, Vives-Gilabert Y, Crespo I, Portella MJ, de Juan-Delago M & Webb SM. Hippocampal dysfunction in cured Cushing's syndrome patients, detected by 1H-MR-spectroscopy. Clinical Endocrinology 2013 79 700-707. (doi:10.1111/cen.12224)
19. Santos A, Resmini E, Crespo I, Pires P, Vives-Gilabert Y, Granell E, Valassi E, Gomez-Anson B, Martinez-Momblan MA, Mataro M et al. Small cerebellar cortex volume in patients with active Cushing's syndrome. European Journal of Endocrinology 2014 171 461-469. (doi:10.1530/EJE-14-0371)
20. Simmons NE, Do HM, Lipper MH & Laws ER Jr. Cerebral atrophy in Cushing's disease. Surgical Neurology 2000 53 72-76. (doi:10.1016/S0090-3019(99)00197-4)
21. Starkman MN, Giordani B, Gebarski SS & Schteingart DE. Improvement in mood and ideation associated with increase in right caudate volume. Journal of Affective Disorders 2007 101 139-147. (doi:10.1016/j.jad.2006.11.007)
22. Andela CD, van der Werff SJ, Pannekoek JN, van den Berg SM, Meijer OC, van Buchem MA, Rombouts SA, van der Mast RC, Romijn JA, Tiemensma J et al. Smaller grey matter volumes in the anterior cingulate cortex and greater cerebellar volumes in patients with long-term remission of Cushing's disease: a case-control study. European Journal of Endocrinology 2013 169 811-819. (doi:10.1530/EJE-13-0471)
23. Khiat A, Bard C, Lacroix A, Rousseau J & Boulanger Y. Brain metabolic alterations in Cushing's syndrome as monitored by proton magnetic resonance spectroscopy. NMR in Biomedicine 1999 12 357-363. (doi:10.1002/(SICI)1099-1492(199910)12:6〈357::AID-NBM584〉3.0.CO;2-U)
24. Khiat A, Bard C, Lacroix A & Boulanger Y. Recovery of the brain choline level in treated Cushing's patients as monitored by proton magnetic resonance spectroscopy. Brain Research 2000 862 301-307. (doi:10.1016/S0006-8993(00)02147-8)
25. Langenecker SA, Weisenbach SL, Giordani B, Briceno EM, Guidotti Breting LM, Schallmo MP, Leon HM, Noll DC, Zubieta JK, Schteingart DE et al. Impact of chronic hypercortisolemia on affective processing. Neuropharmacology 2012 62 217-225. (doi:10.1016/j.neuropharm.2011.07.006)
26. Maheu FS, Mazzone L, Merke DP, Keil MF, Stratakis CA, Pine DS &Ernst M. Altered amygdala and hippocampus function in adolescents with hypercortisolemia: a functional magnetic resonance imaging study of Cushing syndrome. Development and Psychopathology 2008 20 1177-1189. (doi:10.1017/S0954579408000564)
27. Merke DP, Giedd JN, Keil MF, Mehlinger SL, Wiggs EA, Holzer S, Rawson E, Vaituzis AC, Stratakis CA & Chrousos GP. Children experience cognitive decline despite reversal of brain atrophy one year after resolution of Cushing syndrome. Journal of Clinical Endocrinology and Metabolism 2005 90 2531-2536. (doi:10.1210/jc.2004-2488)
28. Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, Costa RM & Sousa N. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009 325 621-625. (doi:10.1126/science.1171203)
29. van der Werff SJ, Andela CD, Nienke PJ, Meijer OC, van Buchem MA, Rombouts SA, van der Mast RC, Biermasz NR, Pereira AM & van der Wee NJ. Widespread reductions of white matter integrity in patients with long-term remission of Cushing's disease. NeuroImage. Clinical 2014 4 659-667. (doi:10.1016/j.nicl.2014.01.017)
30. Hook JN, Giordani B, Schteingart DE, Guire K, Giles J, Ryan K, Gebarski SS, Langenecker SA & Starkman MN. Patterns of cognitive change over time and relationship to age following successful treatment of Cushing's disease. Journal of the International Neuropsychological Society 2007 13 21-29. (doi:10.1017/S1355617707070051)
31. Paisley AN, Rowles SV, Roberts ME, Webb SM, Badia X, Prieto L, Shalet SM & Trainer PJ. Treatment of acromegaly improves quality of life, measured by AcroQol. Clinical Endocrinology 2007 67 358-362. (doi:10.1111/j.1365-2265.2007.02891.x)
32. Martignoni E, Costa A, Sinforiani E, Liuzzi A, Chiodini P, Mauri M, Bono G & Nappi G. The brain as a target for adrenocortical steroids: cognitive implications. Psychoneuroendocrinology 1992 17 343-354. (doi:10.1016/0306-4530(92)90040-E)
33. Toffanin T, Nifosi F, Follador H, Passamani A, Zonta F, Ferri G, Scanarini M, Amista P, Pigato G, Scaroni C et al. Volumetric MRI analysis of hippocampal subregions in Cushing's disease: a model for glucocorticoid neural modulation. European Psychiatry 2011 26 64-67. (doi:10.1016/j.eurpsy.2010.09.003)
34. Tiemensma J, Biermasz NR, Middelkoop HA, van der Mast RC, Romijn JA & Pereira AM. Increased prevalence of psychopathology and maladaptive personality traits after long-term cure of Cushing's disease. Journal of Clinical Endocrinology and Metabolism 2010 95 E129-E141. (doi:10.1210/jc.2010-0512)
35. De Kloet ER, Joels M & Holsboer F. Stress and the brain: from adaptation to disease. Nature Reviews. Neuroscience 2005 6 463-475. (doi:10.1038/nrn1683)
36. De Kloet ER, Vreugdenhil E, Oitzl MS & Joels M. Brain corticosteroid receptor balance in health and disease. Endocrine Reviews 1998 19 269-301. (doi:10.1210/edrv.19.3.0331)
37. Schubert MI, Kalisch R, Sotiropoulos I, Catania C, Sousa N, Almeida OF & Auer DP. Effects of altered corticosteroid milieu on rat hippocampal neurochemistry and structure - an in vivo magnetic resonance spectroscopy and imaging study. Journal of Psychosomatic Research 2008 42 902-912. (doi:10.1016/j.jpsychires.2007.10.003)
38. Cerqueira JJ, Catania C, Sotiropoulos I, Schubert M, Kalisch R, Almeida OF, Auer DP & Sousa N. Corticosteroid status influences the volume of the rat cingulate cortex - a magnetic resonance imaging study. Journal of Psychosomatic Research 2005 39 451-460. (doi:10.1016/j.jpsychires.2005.01.003)
39. Oomen CA, Mayer JL, De Kloet ER, Joels M & Lucassen PJ. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. European Journal of Neuroscience 2007 26 3395-3401. (doi:10.1111/j.1460-9568.2007.05972.x)
40. Leon-Carrion J, Atutxa AM, Mangas MA, Soto-Moreno A, Pumar A, Leon-Justel A, Martin-Rodriguez JF, Venegas E, Dominguez-Morales MR & Leal-Cerro A. A clinical profile of memory impairment in humans due to endogenous glucocorticoid excess. Clinical Endocrinology 2009 70 192-200. (doi:10.1111/j.1365-2265.2008.03355.x)
41. Michaud K, Forget H & Cohen H. Chronic glucocorticoid hypersecretion in Cushing's syndrome exacerbates cognitive aging. Brain and Cognition 2009 71 1-8. (doi:10.1016/j.bandc.2009.02.013)
42. Shin LM & Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010 35 169-191. (doi:10.1038/npp.2009.83)
43. Brown ES, Woolston J, Frol A, Bobadilla L, Khan DA, Hanczyc M, Rush AJ, Fleckenstein J, Babcock E & Cullum CM. Hippocampal volume, spectroscopy, cognition, and mood in patients receiving corticosteroid therapy. Biological Psychiatry 2004 55 538-545. (doi:10.1016/j.biopsych.2003.09.010)
44. Brown ES, Woolston DJ & Frol AB. Amygdala volume in patients receiving chronic corticosteroid therapy. Biological Psychiatry 2008 63 705-709. (doi:10.1016/j.biopsych.2007.09.014)
45. Bentson J, Reza M, Winter J & Wilson G. Steroids and apparent cerebral atrophy on computed tomography scans. Journal of Computer Assisted Tomography 1978 2 16-23. (doi:10.1097/00004728-197801000-00003)
46. Khiat A, Yared Z, Bard C, Lacroix A & Boulanger Y. Long-term brain metabolic alterations in exogenous Cushing's syndrome as monitored by proton magnetic resonance spectroscopy. Brain Research 2001 911 134-140. (doi:10.1016/S0006-8993(01)02697-X)
47. Cherrier MM. Testosterone effects on cognition in health and disease. Frontiers of Hormone Research 2009 37 150-162. (doi:10.1159/000176051)
48. Amin Z, Gueorguieva R, Cappiello A, Czarkowski KA, Stiklus S, Anderson GM, Naftolin F & Epperson CN. Estradiol and tryptophan depletion interact to modulate cognition in menopausal women. Neuropsychopharmacology 2006 31 2489-2497. (doi:10.1038/sj.npp.1301114)
49. Bauer M, Goetz T, Glenn T & Whybrow PC. The thyroid-brain interaction in thyroid disorders and mood disorders. Journal of Neuroendocrinology 2008 20 1101-1114. (doi:10.1111/j.1365-2826.2008.01774.x)
50. Geijselaers SL, Sep SJ, Stehouwer CD & Biessels GJ. Glucose regulation, cognition, and brain MRI in type 2 diabetes: a systematic review. Lancet. Diabetes & Endocrinology 2015 3 75-89. (doi:10.1016/S2213-8587(14)70148-2)
51. Hajjar I, Quach L, Yang F, Chaves PH, Newman AB, Mukamal K, Longstreth W Jr, Inzitari M & Lipsitz LA. Hypertension, white matter hyperintensities, and concurrent impairments in mobility, cognition, and mood: the Cardiovascular Health Study. Circulation 2011 123 858-865. (doi:10.1161/CIRCULATIONAHA.110.978114)