Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Research Article

Prospective Investigation of Glutamate Levels and Percentage Gray Matter in the Medial Prefrontal Cortex in Females at Risk for Postpartum Depression

Author(s): Arjun Ghuman*, Alyssa McEwen*, Kim Hoang Tran, Nicholas Mitchell, Chris Hanstock, Peter Seres, Gian Jhangri, Denee Burgess, Glen Baker and Jean-Michel Le Melledo

Volume 20, Issue 10, 2022

Published on: 21 June, 2022

Page: [1988 - 2000] Pages: 13

DOI: 10.2174/1570159X20666220302101115

Price: $65

conference banner
Abstract

Background: The substantial female hormone fluctuations associated with pregnancy and postpartum have been linked to a greater risk of developing depressive symptoms, particularly in high-risk women (HRW), i.e. those with histories of mood sensitivity to female hormone fluctuations. We have shown that glutamate (Glu) levels in the medial prefrontal cortex (MPFC) decrease during perimenopause, a period of increased risk of developing a major depressive episode. Our team has also demonstrated that percentage gray matter (%GM), another neural correlate of maternal brain health, decreases in the MPFC during pregnancy.

Objective: To investigate MPFC Glu levels and %GM from late pregnancy up to 7 weeks postpartum in HRW and healthy pregnant women (HPW).

Methods: Single-voxel spectra were acquired from the MPFC of 41 HPW and 22 HRW using 3- Tesla in vivo proton magnetic resonance spectroscopy at five different time points.

Results: We observed a statistically significant interaction between time and group for the metabolite Glu, with Glu levels being lower for HRW during pregnancy and early postpartum (p<0.05). MPFC %GM was initially lower during pregnancy and then significantly increased over time in both groups (p<0.01).

Conclusion: This investigation suggests that the vulnerability towards PPD is associated with unique fluctuations of MPFC Glu levels during pregnancy and early postpartum period. Our results also suggest that the decline in MPFC %GM associated with pregnancy seems to progressively recover over time. Further investigations are needed to determine the specific role that female hormones play on the physiological changes in %GM during pregnancy and postpartum.

Keywords: Glutamate, pregnancy, postpartum, depression, magnetic resonance spectroscopy, gray matter.

Graphical Abstract

[1]
Gaynes, BN; Gavin, N Meltzer-Brody, S Perinatal depression: Prevalence, screening accuracy, and screening outcomes: Summary. AHRQ Evidence Report Summaries. 2005.
[2]
Edition, F. Diagnostic and statistical manual of mental disorders. Am Psychiatric Assoc, 2013, 21.
[3]
Leahy-Warren, P.; McCarthy, G.; Corcoran, P. Postnatal depression in first-time mothers: Prevalence and relationships between functional and structural social support at 6 and 12 weeks postpartum. Arch. Psychiatr. Nurs., 2011, 25(3), 174-184.
[http://dx.doi.org/10.1016/j.apnu.2010.08.005] [PMID: 21621731]
[4]
Mori, T.; Tsuchiya, K.J.; Matsumoto, K.; Suzuki, K.; Mori, N.; Takei, N. Psychosocial risk factors for postpartum depression and their relation to timing of onset: The Hamamatsu Birth Cohort (HBC) Study. J. Affect. Disord., 2011, 135(1-3), 341-346.
[http://dx.doi.org/10.1016/j.jad.2011.07.012] [PMID: 21824663]
[5]
Bloch, M.; Rotenberg, N.; Koren, D.; Klein, E. Risk factors for early postpartum depressive symptoms. Gen. Hosp. Psychiatry, 2006, 28(1), 3-8.
[http://dx.doi.org/10.1016/j.genhosppsych.2005.08.006] [PMID: 16377359]
[6]
Tronick, E.; Reck, C. Infants of depressed mothers. Harv. Rev. Psychiatry, 2009, 17(2), 147-156.
[http://dx.doi.org/10.1080/10673220902899714] [PMID: 19373622]
[7]
Josefsson, A.; Berg, G.; Nordin, C.; Sydsjö, G. Prevalence of depressive symptoms in late pregnancy and postpartum. Acta Obstet. Gynecol. Scand., 2001, 80(3), 251-255.
[http://dx.doi.org/10.1034/j.1600-0412.2001.080003251.x] [PMID: 11207491]
[8]
Stowe, Z.N.; Hostetter, A.L.; Newport, D.J. The onset of postpartum depression: Implications for clinical screening in obstetrical and primary care. Am. J. Obstet. Gynecol., 2005, 192(2), 522-526.
[http://dx.doi.org/10.1016/j.ajog.2004.07.054] [PMID: 15695997]
[9]
Pittenger, C.; Sanacora, G.; Krystal, J.H. The NMDA receptor as a therapeutic target in major depressive disorder. CNS Neurol. Disord. Drug Targets, 2007, 6(2), 101-115.
[http://dx.doi.org/10.2174/187152707780363267] [PMID: 17430148]
[10]
Mitchell, N.D.; Baker, G.B. An update on the role of glutamate in the pathophysiology of depression. Acta Psychiatr. Scand., 2010, 122(3), 192-210.
[http://dx.doi.org/10.1111/j.1600-0447.2009.01529.x] [PMID: 20105149]
[11]
Berman, R.M.; Cappiello, A.; Anand, A.; Oren, D.A.; Heninger, G.R.; Charney, D.S.; Krystal, J.H. Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry, 2000, 47(4), 351-354.
[http://dx.doi.org/10.1016/S0006-3223(99)00230-9] [PMID: 10686270]
[12]
Zarate, C.A., Jr; Singh, J.B.; Carlson, P.J.; Brutsche, N.E.; Ameli, R.; Luckenbaugh, D.A.; Charney, D.S.; Manji, H.K. A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry, 2006, 63(8), 856-864.
[http://dx.doi.org/10.1001/archpsyc.63.8.856] [PMID: 16894061]
[13]
Lazarevic, V.; Yang, Y.; Flais, I.; Svenningsson, P. Ketamine decreases neuronally released glutamate via retrograde stimulation of presynaptic adenosine A1 receptors. Mol. Psychiatry, 2021, 26(12), 7425-7435.
[http://dx.doi.org/10.1038/s41380-021-01246-3] [PMID: 34376822]
[14]
Luykx, J.J.; Laban, K.G.; van den Heuvel, M.P.; Boks, M.P.; Mandl, R.C.; Kahn, R.S.; Bakker, S.C. Region and state specific glutamate downregulation in major depressive disorder: A meta-analysis of (1)H-MRS findings. Neurosci. Biobehav. Rev., 2012, 36(1), 198-205.
[http://dx.doi.org/10.1016/j.neubiorev.2011.05.014] [PMID: 21672551]
[15]
Yüksel, C.; Öngür, D. Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol. Psychiatry, 2010, 68(9), 785-794.
[http://dx.doi.org/10.1016/j.biopsych.2010.06.016] [PMID: 20728076]
[16]
Arnone, D.; Mumuni, A.N.; Jauhar, S.; Condon, B.; Cavanagh, J. Indirect evidence of selective glial involvement in glutamate-based mechanisms of mood regulation in depression: Meta-analysis of absolute prefrontal neuro-metabolic concentrations. Eur. Neuropsychopharmacol., 2015, 25(8), 1109-1117.
[http://dx.doi.org/10.1016/j.euroneuro.2015.04.016] [PMID: 26028038]
[17]
Moriguchi, S.; Takamiya, A.; Noda, Y.; Horita, N.; Wada, M.; Tsugawa, S.; Plitman, E.; Sano, Y.; Tarumi, R.; ElSalhy, M.; Katayama, N.; Ogyu, K.; Miyazaki, T.; Kishimoto, T.; Graff-Guerrero, A.; Meyer, J.H.; Blumberger, D.M.; Daskalakis, Z.J.; Mimura, M.; Nakajima, S. Glutamatergic neurometabolite levels in major depressive disorder: A systematic review and meta-analysis of proton magnetic resonance spectroscopy studies. Mol. Psychiatry, 2019, 24(7), 952-964.
[http://dx.doi.org/10.1038/s41380-018-0252-9] [PMID: 30315224]
[18]
Kantrowitz, J.T.; Dong, Z.; Milak, M.S.; Rashid, R.; Kegeles, L.S.; Javitt, D.C.; Lieberman, J.A.; John Mann, J. Ventromedial prefrontal cortex/anterior cingulate cortex Glx, glutamate, and GABA levels in medication-free major depressive disorder. Transl. Psychiatry, 2021, 11(1), 419.
[http://dx.doi.org/10.1038/s41398-021-01541-1] [PMID: 34354048]
[19]
Godlewska, B.R.; Clare, S.; Cowen, P.J.; Emir, U.E. Ultra-high-field magnetic resonance spectroscopy in psychiatry. Front. Psychiatry, 2017, 8, 123.
[http://dx.doi.org/10.3389/fpsyt.2017.00123] [PMID: 28744229]
[20]
Tkác, I.; Öz, G.; Adriany, G.; Uğurbil, K.; Gruetter, R. In vivo 1H NMR spectroscopy of the human brain at high magnetic fields: Metabolite quantification at 4T vs . 7T. Magn. Reson. Med., 2009, 62(4), 868-879.
[http://dx.doi.org/10.1002/mrm.22086] [PMID: 19591201]
[21]
McEwen, A.M.; Burgess, D.T.; Hanstock, C.C.; Seres, P.; Khalili, P.; Newman, S.C.; Baker, G.B.; Mitchell, N.D.; Khudabux-Der, J.; Allen, P.S.; LeMelledo, J.M. Increased glutamate levels in the medial prefrontal cortex in patients with postpartum depression. Neuropsychopharmacol., 2012, 37(11), 2428-2435.
[http://dx.doi.org/10.1038/npp.2012.101] [PMID: 22805604]
[22]
McEwen, A.M.; Burgess, D.T.A.; Hanstock, S.E.C.; Hanstock, C.C.; Seres, P.; Khalili, P.; Newman, S.C.; Baker, G.B.; Mitchell, N.D.; Allen, P.S.; Le Melledo, J.M. Glutamate levels in the medial prefrontal cortex of healthy pregnant women compared to non-pregnant controls. Psychoneuroendocrinol., 2021, 133, 105382.
[http://dx.doi.org/10.1016/j.psyneuen.2021.105382] [PMID: 34419762]
[23]
Sanacora, G.; Gueorguieva, R.; Epperson, C.N.; Wu, Y.T.; Appel, M.; Rothman, D.L.; Krystal, J.H.; Mason, G.F. Subtype-specific alterations of γ-aminobutyric acid and glutamate in patients with major depression. Arch. Gen. Psychiatry, 2004, 61(7), 705-713.
[http://dx.doi.org/10.1001/archpsyc.61.7.705] [PMID: 15237082]
[24]
Truong, V.; Cheng, P.Z.; Lee, H.C.; Lane, T.J.; Hsu, T.Y.; Duncan, N.W. Occipital gamma-aminobutyric acid and glutamate-glutamine alterations in major depressive disorder: An mrs study and meta-analysis. Psychiatry Res. Neuroimaging, 2021, 308, 111238.
[http://dx.doi.org/10.1016/j.pscychresns.2020.111238] [PMID: 33385764]
[25]
Haroon, E.; Fleischer, C.C.; Felger, J.C.; Chen, X.; Woolwine, B.J.; Patel, T.; Hu, X.P.; Miller, A.H. Conceptual convergence: Increased inflammation is associated with increased basal ganglia glutamate in patients with major depression. Mol. Psychiatry, 2016, 21(10), 1351-1357.
[http://dx.doi.org/10.1038/mp.2015.206] [PMID: 26754953]
[26]
Hasler, G.; Fromm, S.; Carlson, P.J.; Luckenbaugh, D.A.; Waldeck, T.; Geraci, M.; Roiser, J.P.; Neumeister, A.; Meyers, N.; Charney, D.S.; Drevets, W.C. Neural response to catecholamine depletion in unmedicated subjects with major depressive disorder in remission and healthy subjects. Arch. Gen. Psychiatry, 2008, 65(5), 521-531.
[http://dx.doi.org/10.1001/archpsyc.65.5.521] [PMID: 18458204]
[27]
Portella, M.J.; de Diego-Adeliño, J.; Gómez-Ansón, B.; Morgan-Ferrando, R.; Vives, Y.; Puigdemont, D.; Pérez-Egea, R.; Ruscalleda, J. Enric Álvarez; Pérez, V. Ventromedial prefrontal spectroscopic abnormalities over the course of depression: A comparison among first episode, remitted recurrent and chronic patients. J. Psychiatr. Res., 2011, 45(4), 427-434.
[http://dx.doi.org/10.1016/j.jpsychires.2010.08.010] [PMID: 20875647]
[28]
Bloch, M.; Daly, R.C.; Rubinow, D.R. Endocrine factors in the etiology of postpartum depression. Compr. Psychiatry, 2003, 44(3), 234-246.
[http://dx.doi.org/10.1016/S0010-440X(03)00034-8] [PMID: 12764712]
[29]
Buckwalter, J.G.; Stanczyk, F.Z.; McCleary, C.A.; Bluestein, B.W.; Buckwalter, D.K.; Rankin, K.P.; Chang, L.; Goodwin, T.M. Pregnancy, the postpartum, and steroid hormones: Effects on cognition and mood. Psychoneuroendocrinol., 1999, 24(1), 69-84.
[http://dx.doi.org/10.1016/S0306-4530(98)00044-4] [PMID: 10098220]
[30]
Lin, T.J.; Lin, S.C.; Erlenmeyer, F.; Kline, I.T.; Underwood, R.; Billiar, R.B.; Little, B. Progesterone production rates during the third trimester of pregnancy in normal women, diabetic women, and women with abnormal glucose tolerance. J. Clin. Endocrinol. Metab., 1972, 34(2), 287-297.
[http://dx.doi.org/10.1210/jcem-34-2-287]
[31]
Tulchinsky, D.; Okada, D.M. Hormones in human pregnancy. IV. Plasma progesterone. Am. J. Obstet. Gynecol., 1975, 121(3), 293-299.
[http://dx.doi.org/10.1016/0002-9378(75)90001-0] [PMID: 163589]
[32]
Batra, N.A.; Seres-Mailo, J.; Hanstock, C.; Seres, P.; Khudabux, J.; Bellavance, F.; Baker, G.; Allen, P.; Tibbo, P.; Hui, E.; Le Melledo, J.M. Proton magnetic resonance spectroscopy measurement of brain glutamate levels in premenstrual dysphoric disorder. Biol. Psychiatry, 2008, 63(12), 1178-1184.
[http://dx.doi.org/10.1016/j.biopsych.2007.10.007] [PMID: 18061146]
[33]
Cohen, L.S.; Soares, C.N.; Vitonis, A.F.; Otto, M.W.; Harlow, B.L. Risk for new onset of depression during the menopausal transition: The Harvard study of moods and cycles. Arch. Gen. Psychiatry, 2006, 63(4), 385-390.
[http://dx.doi.org/10.1001/archpsyc.63.4.385] [PMID: 16585467]
[34]
Yap, S.; Luki, J.; Hanstock, C.C.; Seres, P.; Shandro, T.; Hanstock, S.E.C.; Lirette, A.; Zhao, H.H.; Aitchison, K.J.; Le Melledo, J.M. Decreased medial prefrontal cortex glutamate levels in perimenopausal women. Front. Psychiatry, 2021, 12, 763562.
[http://dx.doi.org/10.3389/fpsyt.2021.763562] [PMID: 34966302]
[35]
Davies, S.J.; Lum, J.A.; Skouteris, H.; Byrne, L.K.; Hayden, M.J. Cognitive impairment during pregnancy: A meta-analysis. Med. J. Aust., 2018, 208(1), 35-40.
[http://dx.doi.org/10.5694/mja17.00131] [PMID: 29320671]
[36]
First, M.B.; Williams Janet, B.W.; Spitzer, R.L.; Gibbon, M. Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient editions, SCID I/P. American Psychiatric Publishing Inc; 2002. Available from: https://eprovide.mapi-trust.org/instruments/structured-clinical-interview-for-dsm-iv-axis-i-disorders#member_access_content Accessed August 26, 2021.
[37]
Gruetter, R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med., 1993, 29(6), 804-811.
[http://dx.doi.org/10.1002/mrm.1910290613] [PMID: 8350724]
[38]
Thompson, R.B.; Allen, P.S. Response of metabolites with coupled spins to the STEAM sequence. Magn. Reson. Med., 2001, 45(6), 955-965.
[http://dx.doi.org/10.1002/mrm.1128] [PMID: 11378872]
[39]
Behar, K.L.; Rothman, D.L.; Spencer, D.D.; Petroff, O.A. Analysis of macromolecule resonances in 1H NMR spectra of human brain. Magn. Reson. Med., 1994, 32(3), 294-302.
[http://dx.doi.org/10.1002/mrm.1910320304] [PMID: 7984061]
[40]
Zhu, G.; Gheorghiu, D.; Allen, P.S. Motional degradation of metabolite signal strengths when using STEAM: A correction method. NMR Biomed., 1992, 5(4), 209-211.
[http://dx.doi.org/10.1002/nbm.1940050408] [PMID: 1449957]
[41]
Provencher, S.W. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med., 1993, 30(6), 672-679.
[http://dx.doi.org/10.1002/mrm.1910300604] [PMID: 8139448]
[42]
Pearson Murphy, B.E.; Steinberg, S.I.; Hu, F.Y.; Allison, C.M. Neuroactive ring A-reduced metabolites of progesterone in human plasma during pregnancy: Elevated levels of 5 α- dihydroprogesterone in depressed patients during the latter half of pregnancy. J. Clin. Endocrinol. Metab., 2001, 86(12), 5981-5987.
[PMID: 11739473]
[43]
Carver, C.M.; Reddy, D.S. Neurosteroid interactions with synaptic and extrasynaptic GABA(A) receptors: Regulation of subunit plasticity, phasic and tonic inhibition, and neuronal network excitability. Psychopharmacology (Berl.), 2013, 230(2), 151-188.
[http://dx.doi.org/10.1007/s00213-013-3276-5] [PMID: 24071826]
[44]
Edinoff, A.N.; Odisho, A.S.; Lewis, K.; Kaskas, A.; Hunt, G.; Cornett, E.M.; Kaye, A.D.; Kaye, A.; Morgan, J.; Barrilleaux, P.S.; Lewis, D.; Viswanath, O.; Urits, I. Brexanolone, a GABAA Modulator, in the treatment of postpartum depression in adults: A comprehensive review. Front. Psychiatry, 2021, 12, 699740.
[http://dx.doi.org/10.3389/fpsyt.2021.699740] [PMID: 34594247]
[45]
Kanes, S.J.; Colquhoun, H.; Doherty, J.; Raines, S.; Hoffmann, E.; Rubinow, D.R.; Meltzer-Brody, S. Open-label, proof-of-concept study of brexanolone in the treatment of severe postpartum depression. Hum. Psychopharmacol., 2017, 32(2), e2576.
[http://dx.doi.org/10.1002/hup.2576] [PMID: 28370307]
[46]
Chang, Y.; Hsieh, H.L.; Huang, S.K.; Wang, S.J. Neurosteroid allopregnanolone inhibits glutamate release from rat cerebrocortical nerve terminals. Synapse, 2019, 73(3), e22076.
[http://dx.doi.org/10.1002/syn.22076] [PMID: 30362283]
[47]
Hu, A.Q.; Wang, Z.M.; Lan, D.M.; Fu, Y.M.; Zhu, Y.H.; Dong, Y.; Zheng, P. Inhibition of evoked glutamate release by neurosteroid allopregnanolone via inhibition of L-type calcium channels in rat medial prefrontal cortex. Neuropsychopharmacol., 2007, 32(7), 1477-1489.
[http://dx.doi.org/10.1038/sj.npp.1301261] [PMID: 17151597]
[48]
Klak, J.; Hill, M.; Parízek, A.; Havlíková, H.; Bicíková, M.; Hampl, R.; Fait, T.; Sulcová, J.; Pouzar, V.; Kancheva, R.; Stárka, L. Pregnanolone isomers, pregnenolone and their polar conjugates around parturition. Physiol. Res., 2003, 52(2), 211-221.
[PMID: 12678664]
[49]
Lee, K.H.; Cho, J.H.; Choi, I.S.; Park, H.M.; Lee, M.G.; Choi, B.J.; Jang, I.S. Pregnenolone sulfate enhances spontaneous glutamate release by inducing presynaptic Ca2+-induced Ca2+ release. Neuroscience, 2010, 171(1), 106-116.
[http://dx.doi.org/10.1016/j.neuroscience.2010.07.057] [PMID: 20816925]
[50]
Yokomaku, D.; Numakawa, T.; Numakawa, Y.; Suzuki, S.; Matsumoto, T.; Adachi, N.; Nishio, C.; Taguchi, T.; Hatanaka, H. Estrogen enhances depolarization-induced glutamate release through activation of phosphatidylinositol 3-kinase and mitogen-activated protein kinase in cultured hippocampal neurons. Mol. Endocrinol., 2003, 17(5), 831-844.
[http://dx.doi.org/10.1210/me.2002-0314] [PMID: 12554763]
[51]
Smith, S.S.; Waterhouse, B.D.; Chapin, J.K.; Woodward, D.J. Progesterone alters GABA and glutamate responsiveness: A possible mechanism for its anxiolytic action. Brain Res., 1987, 400(2), 353-359.
[http://dx.doi.org/10.1016/0006-8993(87)90634-2] [PMID: 2880640]
[52]
Taylor, M.J.; Selvaraj, S.; Norbury, R.; Jezzard, P.; Cowen, P.J. Normal glutamate but elevated myo-inositol in anterior cingulate cortex in recovered depressed patients. J. Affect. Disord., 2009, 119(1-3), 186-189.
[http://dx.doi.org/10.1016/j.jad.2009.02.022] [PMID: 19324421]
[53]
Price, R.B.; Shungu, D.C.; Mao, X.; Nestadt, P.; Kelly, C.; Collins, K.A.; Murrough, J.W.; Charney, D.S.; Mathew, S.J. Amino acid neurotransmitters assessed by proton magnetic resonance spectroscopy: Relationship to treatment resistance in major depressive disorder. Biol. Psychiatry, 2009, 65(9), 792-800.
[http://dx.doi.org/10.1016/j.biopsych.2008.10.025] [PMID: 19058788]
[54]
Taylor, M.J.; Mannie, Z.N.; Norbury, R.; Near, J.; Cowen, P.J. Elevated cortical glutamate in young people at increased familial risk of depression. Int. J. Neuropsychopharmacol., 2011, 14(2), 255-259.
[http://dx.doi.org/10.1017/S1461145710001094] [PMID: 20846462]
[55]
Albrecht, J.; Sidoryk-Węgrzynowicz, M.; Zielińska, M.; Aschner, M. Roles of glutamine in neurotransmission. Neuron Glia Biol., 2010, 6(4), 263-276.
[http://dx.doi.org/10.1017/S1740925X11000093] [PMID: 22018046]
[56]
Hyder, F.; Rothman, D.L. Advances in imaging brain metabolism. Annu. Rev. Biomed. Eng., 2017, 19(1), 485-515.
[http://dx.doi.org/10.1146/annurev-bioeng-071516-044450] [PMID: 28633562]
[57]
Steel, A.; Mikkelsen, M.; Edden, R.A.E.; Robertson, C.E. Regional balance between glutamate+glutamine and GABA+ in the resting human brain. Neuroimage, 2020, 220, 117112.
[http://dx.doi.org/10.1016/j.neuroimage.2020.117112] [PMID: 32619710]
[58]
Oatridge, A.; Holdcroft, A.; Saeed, N.; Hajnal, J.V.; Puri, B.K.; Fusi, L.; Bydder, G.M. Change in brain size during and after pregnancy: Study in healthy women and women with preeclampsia. AJNR Am. J. Neuroradiol., 2002, 23(1), 19-26.
[PMID: 11827871]
[59]
Kim, P.; Leckman, J.F.; Mayes, L.C.; Feldman, R.; Wang, X.; Swain, J.E. The plasticity of human maternal brain: Longitudinal changes in brain anatomy during the early postpartum period. Behav. Neurosci., 2010, 124(5), 695-700.
[http://dx.doi.org/10.1037/a0020884] [PMID: 20939669]
[60]
Hoekzema, E.; Barba-Müller, E.; Pozzobon, C.; Picado, M.; Lucco, F.; García-García, D.; Soliva, J.C.; Tobeña, A.; Desco, M.; Crone, E.A.; Ballesteros, A.; Carmona, S.; Vilarroya, O. Pregnancy leads to long-lasting changes in human brain structure. Nat. Neurosci., 2017, 20(2), 287-296.
[http://dx.doi.org/10.1038/nn.4458] [PMID: 27991897]
[61]
Peper, J.S.; Hulshoff Pol, H.E.; Crone, E.A.; van Honk, J. Sex steroids and brain structure in pubertal boys and girls: A mini-review of neuroimaging studies. Neuroscience, 2011, 191, 28-37.
[http://dx.doi.org/10.1016/j.neuroscience.2011.02.014] [PMID: 21335066]
[62]
Zubiaurre-Elorza, L.; Junque, C.; Gómez-Gil, E.; Guillamon, A. Effects of cross-sex hormone treatment on cortical thickness in transsexual individuals. J. Sex. Med., 2014, 11(5), 1248-1261.
[http://dx.doi.org/10.1111/jsm.12491] [PMID: 24617977]
[63]
Rutherford, J.M.; Moody, A.; Crawshaw, S.; Rubin, P.C. Magnetic resonance spectroscopy in pre-eclampsia: Evidence of cerebral ischaemia. BJOG, 2003, 110(4), 416-423.
[http://dx.doi.org/10.1046/j.1471-0528.2003.00416.x] [PMID: 12699805]
[64]
Caudill, M.A. Pre- and postnatal health: Evidence of increased choline needs. J. Am. Diet. Assoc., 2010, 110(8), 1198-1206.
[http://dx.doi.org/10.1016/j.jada.2010.05.009] [PMID: 20656095]
[65]
Girard, N.; Gouny, S.C.; Viola, A.; Le Fur, Y.; Viout, P.; Chaumoitre, K.; D’Ercole, C.; Gire, C.; Figarella-Branger, D.; Cozzone, P.J. Assessment of normal fetal brain maturation in utero by proton magnetic resonance spectroscopy. Magn. Reson. Med., 2006, 56(4), 768-775.
[http://dx.doi.org/10.1002/mrm.21017] [PMID: 16964617]
[66]
Jansen, J.F.; Backes, W.H.; Nicolay, K.; Kooi, M.E. 1H MR spectroscopy of the brain: Absolute quantification of metabolites. Radiology, 2006, 240(2), 318-332.
[http://dx.doi.org/10.1148/radiol.2402050314] [PMID: 16864664]
[67]
Clements, H.; Duncan, K.R.; Fielding, K.; Gowland, P.A.; Johnson, I.R.; Baker, P.N. Infants exposed to MRI in utero have a normal paediatric assessment at 9 months of age. Br. J. Radiol., 2000, 73(866), 190-194.
[http://dx.doi.org/10.1259/bjr.73.866.10884733] [PMID: 10884733]
[68]
Heerschap, A.; Kok, R.D.; van den Berg, P.P. Antenatal proton MR spectroscopy of the human brain in vivo . Childs Nerv. Syst., 2003, 19(7-8), 418-421.
[http://dx.doi.org/10.1007/s00381-003-0774-5] [PMID: 12811484]
[69]
Kok, R.D.; de Vries, M.M.; Heerschap, A.; van den Berg, P.P. Absence of harmful effects of magnetic resonance exposure at 1.5 T in utero during the third trimester of pregnancy: A follow-up study. Magn. Reson. Imaging, 2004, 22(6), 851-854.
[http://dx.doi.org/10.1016/j.mri.2004.01.047] [PMID: 15234454]
[70]
Kreis, R.; Hofmann, L.; Kuhlmann, B.; Boesch, C.; Bossi, E.; Hüppi, P.S. Brain metabolite composition during early human brain development as measured by quantitative in vivo 1H magnetic resonance spectroscopy. Magn. Reson. Med., 2002, 48(6), 949-958.
[http://dx.doi.org/10.1002/mrm.10304] [PMID: 12465103]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy