Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T18:06:44.511Z Has data issue: false hasContentIssue false
  • English
  • Français

Early-life metal exposure and schizophrenia: A proof-of-concept study using novel tooth-matrix biomarkers

Published online by Cambridge University Press:  23 March 2020

A. Modabbernia ,
E. Velthorst ,
C. Gennings ,
L. De Haan ,
C. Austin ,
A. Sutterland ,
J. Mollon ,
S. Frangou ,
R. Wright  and
M. Arora
...Show all authors
A. Modabbernia*
Affiliation:
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, United States Seaver Center for Autism Research and Treatment, Icahn School of Medicine at Mount Sinai, New York, United States Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
E. Velthorst
Affiliation:
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, United States Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
C. Gennings
Affiliation:
Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
L. De Haan
Affiliation:
Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
C. Austin
Affiliation:
Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
A. Sutterland
Affiliation:
Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
J. Mollon
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology, and Neuroscience, King’s College London, London, England United Kingdom
S. Frangou
Affiliation:
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, United States Psychosis Research Program, Icahn School of Medicine at Mount Sinai, New York, United States
R. Wright
Affiliation:
Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
M. Arora
Affiliation:
Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
A. Reichenberg
Affiliation:
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, United States Seaver Center for Autism Research and Treatment, Icahn School of Medicine at Mount Sinai, New York, United States Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, United States Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, United States
*
⁎Corresponding author at: Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 1 Gustave L. Levy Pl, New York, NY 10029, United States, Amirhossein.modabbernia@mssm.edu.
Get access

Abstract

Background

Despite evidence for the effects of metals on neurodevelopment, the long-term effects on mental health remain unclear due to methodological limitations. Our objective was to determine the feasibility of studying metal exposure during critical neurodevelopmental periods and to explore the association between early-life metal exposure and adult schizophrenia.

Methods

We analyzed childhood-shed teeth from nine individuals with schizophrenia and five healthy controls. We investigated the association between exposure to lead (Pb2+), manganese (Mn2+), cadmium (Cd2+), copper (Cu2+), magnesium (Mg2+), and zinc (Zn2+), and schizophrenia, psychotic experiences, and intelligence quotient (IQ). We reconstructed the dose and timing of early-life metal exposures using laser ablation inductively coupled plasma mass spectrometry.

Results

We found higher early-life Pb2+ exposure among patients with schizophrenia than controls. The differences in log Mn2+ and log Cu2+ changed relatively linearly over time to postnatal negative values. There was a positive correlation between early-life Pb2+ levels and psychotic experiences in adulthood. Moreover, we found a negative correlation between Pb2+ levels and adult IQ.

Conclusions

In our proof-of-concept study, using tooth-matrix biomarker that provides direct measurement of exposure in the fetus and newborn, we provide support for the role of metal exposure during critical neurodevelopmental periods in psychosis.

Keywords

Environmental exposureLeadNeurodevelopmental disordersPsychosisToothTrace elements
Type
Original article
Information
European Psychiatry , Volume 36 , August 2016 , pp. 1 - 6
Copyright
Copyright © European Psychiatric Association 2016

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Weinberger, D.R.Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 1987;44:660–669.CrossRefGoogle ScholarPubMed
Wasserman, G.A., Liu, X., Parvez, F., Ahsan, H., Factor-Litvak, P., Kline, J., et al.Water arsenic exposure and intellectual function in 6-year-old children in Araihazar, Bangladesh. Environ Health Perspect 2007;115:285–289.CrossRefGoogle ScholarPubMed
Jamieson, J.A., Taylor, C.G., Weiler, H.A.Marginal zinc deficiency exacerbates bone lead accumulation and high dietary zinc attenuates lead accumulation at the expense of bone density in growing rats. Toxicol Sci 2006;92:286–294.CrossRefGoogle ScholarPubMed
Needleman, H.L., Gunnoe, C., Leviton, A., Reed, R., Peresie, H., Maher, C., et al.Deficits in psychologic and classroom performance of children with elevated dentine lead levels. N Engl J Med 1979;300:689–695.CrossRefGoogle ScholarPubMed
Bellinger, D., Hu, H., Titlebaum, L., Needleman, H.L.Attentional correlates of dentin and bone lead levels in adolescents. Arch Environ Health 1994;49:98–105.CrossRefGoogle ScholarPubMed
Wright, R.O., Amarasiriwardena, C., Woolf, A.D., Jim, R., Bellinger, D.C.Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology 2006;27:210–216.CrossRefGoogle Scholar
Rodriguez-Barranco, M., Lacasana, M., Gil, F., Lorca, A., Alguacil, J., Rohlman, D.S., et al.Cadmium exposure and neuropsychological development in school children in southwestern Spain. Environ Res 2014;134:66–73.CrossRefGoogle ScholarPubMed
Rodriguez-Barranco, M., Lacasana, M., Aguilar-Garduno, C., Alguacil, J., Gil, F., Gonzalez-Alzaga, B., et al.Association of arsenic, cadmium and manganese exposure with neurodevelopment and behavioural disorders in children: a systematic review and meta-analysis. Sci Total Environ 2013;454–455:562–577.CrossRefGoogle ScholarPubMed
Adamo, A.M., Oteiza, P.I.Zinc deficiency and neurodevelopment: the case of neurons. Biofactors 2010;36:117–124.Google ScholarPubMed
Bellinger, D.C.Very low lead exposures and children’s neurodevelopment. Curr Opin Pediatr 2008;20:172–177.CrossRefGoogle ScholarPubMed
Akil, M., Brewer, G.J.Psychiatric and behavioral abnormalities in Wilson’s disease. Adv Neurol 1995;65:171–178.Google ScholarPubMed
McDonald, L.V., Lake, C.R.Psychosis in an adolescent patient with Wilson’s disease: effects of chelation therapy. Psychosom Med 1995;57:202–204.CrossRefGoogle Scholar
Koh, J.Y., Choi, D.W.Zinc toxicity on cultured cortical neurons: involvement of N-methyl-D-aspartate receptors. Neuroscience 1994;60:1049–1057.CrossRefGoogle ScholarPubMed
Guilarte, T.R.Manganese neurotoxicity: new perspectives from behavioral, neuroimaging, and neuropathological studies in humans and non-human primates. Front Aging Neurosci 2013;5:23CrossRefGoogle ScholarPubMed
Grandjean, P., Landrigan, P.J.Neurobehavioural effects of developmental toxicity. Lancet Neurol 2014;13:330–338.CrossRefGoogle ScholarPubMed
Grandjean, P., Landrigan, P.J.Developmental neurotoxicity of industrial chemicals. Lancet 2006;368:2167–2178.CrossRefGoogle ScholarPubMed
Wasserman, G.A., Liu, X., Parvez, F., Ahsan, H., Factor-Litvak, P., van Geen, A., et al.Water arsenic exposure and children’s intellectual function in Araihazar, Bangladesh. Environ Health Perspect 2004;112:1329–1333.CrossRefGoogle ScholarPubMed
Sandstead, H.H., Penland, J.G., Alcock, N.W., Dayal, H.H., Chen, X.C., Li, J.S., et al.Effects of repletion with zinc and other micronutrients on neuropsychologic performance and growth of Chinese children. Am J Clin Nutr 1998;68:470S–475S.CrossRefGoogle ScholarPubMed
Umamaheswari, K., Bhaskaran, M., Krishnamurthy, G., Vasudevan, H., Vasudevan, K.Effect of iron and zinc deficiency on short term memory in children. Indian Pediatr 2011;48:289–293.CrossRefGoogle ScholarPubMed
Cecil, K.M., Brubaker, C.J., Adler, C.M., Dietrich, K.N., Altaye, M., Egelhoff, J.C., et al.Decreased brain volume in adults with childhood lead exposure. PLoS Med 2008;5:e112CrossRefGoogle ScholarPubMed
Wasserman, G.A., Liu, X., Parvez, F., Factor-Litvak, P., Ahsan, H., Levy, D., et al.Arsenic and manganese exposure and children’s intellectual function. Neurotoxicology 2011;32:450–457.CrossRefGoogle ScholarPubMed
Brubaker, C.J., Schmithorst, V.J., Haynes, E.N., Dietrich, K.N., Egelhoff, J.C., Lindquist, D.M., et al.Altered myelination and axonal integrity in adults with childhood lead exposure: a diffusion tensor imaging study. Neurotoxicology 2009;30:867–875.CrossRefGoogle ScholarPubMed
Neal, A.P., Guilarte, T.R.Molecular neurobiology of lead (Pb(2+)): effects on synaptic function. Mol Neurobiol 2010;42:151–160.CrossRefGoogle ScholarPubMed
Guilarte, T.R., Chen, M.K.Manganese inhibits NMDA receptor channel function: implications to psychiatric and cognitive effects. Neurotoxicology 2007;28:1147–1152.CrossRefGoogle ScholarPubMed
Guilarte, T.R., Opler, M., Pletnikov, M.Is lead exposure in early life an environmental risk factor for Schizophrenia? Neurobiological connections and testable hypotheses. Neurotoxicology 2012;33:560–574.CrossRefGoogle ScholarPubMed
Forrest, C.M., Khalil, O.S., Pisar, M., Darlington, L.G., Stone, T.W.Prenatal inhibition of the tryptophan–kynurenine pathway alters synaptic plasticity and protein expression in the rat hippocampus. Brain Res 2013;1504:1–15.CrossRefGoogle ScholarPubMed
Forrest, C.M., Khalil, O.S., Pisar, M., McNair, K., Kornisiuk, E., Snitcofsky, M., et al.Changes in synaptic transmission and protein expression in the brains of adult offspring after prenatal inhibition of the kynurenine pathway. Neuroscience 2013;254:241–259.CrossRefGoogle ScholarPubMed
Forrest, C.M., McNair, K., Pisar, M., Khalil, O.S., Darlington, L.G., Stone, T.W.Altered hippocampal plasticity by prenatal kynurenine administration, kynurenine-3-monoxygenase (KMO) deletion or galantamine. Neuroscience 2015;310:91–105.CrossRefGoogle ScholarPubMed
Salustri, C., Barbati, G., Ghidoni, R., Quintiliani, L., Ciappina, S., Binetti, G., et al.Is cognitive function linked to serum free copper levels? A cohort study in a normal population. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 2010;121:502–507.CrossRefGoogle Scholar
Rahman, A., Azad, M.A., Hossain, I., Qusar, M.M., Bari, W., Begum, F., et al.Zinc, manganese, calcium, copper, and cadmium level in scalp hair samples of schizophrenic patients. Biol Trace Elem Res 2009;127:102–108.CrossRefGoogle ScholarPubMed
Wolf, T.L., Kotun, J., Meador-Woodruff, J.H.Plasma copper, iron, ceruloplasmin and ferroxidase activity in schizophrenia. Schizophr Res 2006;86:167–171.CrossRefGoogle Scholar
Liu, T., Lu, Q.B., Yan, L., Guo, J., Feng, F., Qiu, J., et al.Comparative study on serum levels of 10 trace elements in schizophrenia. PLoS ONE 2015;10:e0133622CrossRefGoogle Scholar
Yanik, M., Kocyigit, A., Tutkun, H., Vural, H., Herken, H.Plasma manganese, selenium, zinc, copper, and iron concentrations in patients with schizophrenia. Biol Trace Elem Res 2004;98:109–117.CrossRefGoogle ScholarPubMed
Pfeiffer, C.C., Iliev, V.A study of zinc deficiency and copper excess in the schizophrenias. Int Rev Neurobiol 1972;1:141–165.CrossRefGoogle Scholar
Opler, M.G., Brown, A.S., Graziano, J., Desai, M., Zheng, W., Schaefer, C., et al.Prenatal lead exposure, delta-aminolevulinic acid, and schizophrenia. Environ Health Perspect 2004;112:548–552.CrossRefGoogle Scholar
Opler, M.G., Buka, S.L., Groeger, J., McKeague, I., Wei, C., Factor-Litvak, P., et al.Prenatal exposure to lead, delta-aminolevulinic acid, and schizophrenia: further evidence. Environ Health Perspect 2008;116:1586–1590.CrossRefGoogle ScholarPubMed
Korver, N., Quee, P.J., Boos, H.B., Simons, C.J., de Haan, L., investigators G, Genetic Risk and Outcome of Psychosis (GROUP), a multi-site longitudinal cohort study focused on gene-environment interaction: objectives, sample characteristics, recruitment and assessment methods. Int J Methods Psychiatr Res 2012;21:205–221.CrossRefGoogle ScholarPubMed
Stefanis, N.C., Hanssen, M., Smirnis, N.K., Avramopoulos, D.A., Evdokimidis, I.K., Stefanis, C.N., et al.Evidence that three dimensions of psychosis have a distribution in the general population. Psychol Med 2002;32:347–358.CrossRefGoogle ScholarPubMed
Hare, D., Austin, C., Doble, P., Arora, M.Elemental bio-imaging of trace elements in teeth using laser ablation-inductively coupled plasma-mass spectrometry. J Dent 2011;39:397–403.CrossRefGoogle ScholarPubMed
Arora, M., Austin, C.Teeth as a biomarker of past chemical exposure. Curr Opin Pediatr 2013;25:261–267.CrossRefGoogle ScholarPubMed
Coull, B.C.H.B., Wright, R.O., Arora, M.Statistical methods for analyzing critical windows of metal exposures using the tooth biomarker. Int Soc Expo Sci (ISES) 2014Google Scholar
Arora, M., Hare, D., Austin, C., Smith, D.R., Doble, P.Spatial distribution of manganese in enamel and coronal dentine of human primary teeth. Sci Total Environ 2011CrossRefGoogle ScholarPubMed
Arora, M., Kennedy, B.J., Elhlou, S., Pearson, N.J., Walker, D.M., Bayl, P., et al.Spatial distribution of lead in human primary teeth as a biomarker of pre- and neonatal lead exposure. Sci Total Environ 2006;371:55–62.CrossRefGoogle ScholarPubMed
Arora, M., Austin, C., Sarrafpour, B., Hernandez-Avila, M., Hu, H., Wright, R.O., et al.Determining prenatal, early childhood and cumulative long-term lead exposure using micro-spatial deciduous dentine levels. PLoS ONE 2014;9:e97805CrossRefGoogle ScholarPubMed
Arora, M., Bradman, A., Austin, C., Vedar, M., Holland, N., Eskenazi, B., et al.Determining fetal manganese exposure from mantle dentine of deciduous teeth. Environ Sci Technol 2012;46:5118–5125.CrossRefGoogle ScholarPubMed
Austin, C., Smith, T.M., Bradman, A., Hinde, K., Joannes-Boyau, R., Bishop, D., et al.Barium distributions in teeth reveal early-life dietary transitions in primates. Nature 2013;498:216–219.CrossRefGoogle ScholarPubMed
Rodda, J., Okello, A., Edison, P., Dannhauser, T., Brooks, D.J., Walker, Z.(11)C-PIB PET in subjective cognitive impairment. Eur Psychiatry 2010;25:123–125.CrossRefGoogle ScholarPubMed
Ko, J.H., Koshimori, Y., Mizrahi, R., Rusjan, P., Wilson, A.A., Lang, A.E., et al.Voxel-based imaging of translocator protein 18 kDa (TSPO) in high-resolution PET. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab 2013;33:348–350.CrossRefGoogle Scholar
Bauer, M., Romermann, K., Karch, R., Wulkersdorfer, B., Stanek, J., Philippe, C., et al.A pilot PET study to assess the functional interplay between ABCB1 and ABCG2 at the human blood-brain barrier. Clin Pharmacol Ther 2016CrossRefGoogle ScholarPubMed
Park, E., Hwang, Y.M., Chu, M.K., Jung, K.Y.Increased brainstem serotonergic transporter availability in adult migraineurs: an [(18)F]FP-CIT PET imaging pilot study. Nucl Med Mol Imaging 2016;50:70–75.CrossRefGoogle Scholar
Lanphear, B.P., Hornung, R., Khoury, J., Yolton, K., Baghurst, P., Bellinger, D.C., et al.Low-level environmental lead exposure and children’s intellectual function: an international pooled analysis. Environ Health Perspect 2005;113:894–899.CrossRefGoogle ScholarPubMed
Hu, H., Tellez-Rojo, M.M., Bellinger, D., Smith, D., Ettinger, A.S., Lamadrid-Figueroa, H., et al.Fetal lead exposure at each stage of pregnancy as a predictor of infant mental development. Environ Health Perspect 2006;114:1730–1735.CrossRefGoogle ScholarPubMed
Liu, J., Gao, D., Chen, Y., Jing, J., Hu, Q., Chen, Y.Lead exposure at each stage of pregnancy and neurobehavioral development of neonates. Neurotoxicology 2014;44:1–7.CrossRefGoogle ScholarPubMed
Brown, A.S., Schaefer, C.A., Quesenberry, C.P. Jr., Liu, L., Babulas, V.P., Susser, E.S.Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. Am J Psychiatry 2005;162:767–773.CrossRefGoogle ScholarPubMed
Georgieff, M.K.The role of iron in neurodevelopment: fetal iron deficiency and the developing hippocampus. Biochem Soc Trans 2008;36:1267–1271.CrossRefGoogle ScholarPubMed
Meyer-Baron, M., Knapp, G., Schaper, M., van Thriel, C.Performance alterations associated with occupational exposure to manganese – a meta-analysis. Neurotoxicology 2009;30:487–496.CrossRefGoogle ScholarPubMed
Wenisch, E., De Tassigny, A., Trocello, J.M., Beretti, J., Girardot-Tinant, N., Woimant, F.Cognitive profile in Wilson’s disease: a case series of 31 patients. Rev Neurol – France 2013;169:944–949.CrossRefGoogle ScholarPubMed
Medalia, A., Isaacsglaberman, K., Scheinberg, I.H.Neuropsychological impairment in Wilsons-disease. Arch Neurol – Chicago 1988;45:502–504.CrossRefGoogle Scholar
Schendel, D.E., Berg, C.J., Yeargin-Allsopp, M., Boyle, C.A., Decoufle, P.Prenatal magnesium sulfate exposure and the risk for cerebral palsy or mental retardation among very low-birth-weight children aged 3 to 5 years. JAMA 1996;276:1805–1810.CrossRefGoogle ScholarPubMed
Shrestha, K.P., Carrera, A.E.Hair trace elements and mental retardation among children. Arch Environ Health 1988;43:396–398.CrossRefGoogle ScholarPubMed
Slutsky, I., Abumaria, N., Wu, L.J., Huang, C., Zhang, L., Li, B., et al.Enhancement of learning and memory by elevating brain magnesium. Neuron 2010;65:165–177.CrossRefGoogle ScholarPubMed
Ghia, N., Spong, C.Y., Starbuck, V.N., Scialli, A.R., Ghidini, A.Magnesium sulfate therapy affects attention and working memory in patients undergoing preterm labor. Am J Obstet Gynecol 2000;183:940–944.CrossRefGoogle ScholarPubMed
Starobrat-Hermelin, B., Kozielec, T.The effects of magnesium physiological supplementation on hyperactivity in children with attention deficit hyperactivity disorder (ADHD). Positive response to magnesium oral loading test. Magnes Res 1997;10:149–156.Google ScholarPubMed
Alkondon, M., Costa, A.C., Radhakrishnan, V., Aronstam, R.S., Albuquerque, E.X.Selective blockade of NMDA-activated channel currents may be implicated in learning deficits caused by lead. FEBS Lett 1990;261:124–130.CrossRefGoogle ScholarPubMed
Nation, J.R., Frye, G.D., Von Stultz, J., Bratton, G.R.Effects of combined lead and cadmium exposure: changes in schedule-controlled responding and in dopamine, serotonin, and their metabolites. Behav Neurosci 1989;103:1108–1114.CrossRefGoogle ScholarPubMed
Zuch, C.L., O’Mara, D.J., Cory-Slechta, D.A.Low-level lead exposure selectively enhances dopamine overflow in nucleus accumbens: an in vivo electrochemistry time course assessment. Toxicol Appl Pharmacol 1998;150:174–185.CrossRefGoogle Scholar
Andersson, H., Petersson-Grawe, K., Lindqvist, E., Luthman, J., Oskarsson, A., Olson, L.Low-level cadmium exposure of lactating rats causes alterations in brain serotonin levels in the offspring. Neurotoxicol Teratol 1997;19:105–115.CrossRefGoogle ScholarPubMed
Gutierrez-Reyes, E.Y., Albores, A., Rios, C.Increase of striatal dopamine release by cadmium in nursing rats and its prevention by dexamethasone-induced metallothionein. Toxicology 1998;131:145–154.CrossRefGoogle ScholarPubMed
Minami, A., Takeda, A., Nishibaba, D., Takefuta, S., Oku, N.Cadmium toxicity in synaptic neurotransmission in the brain. Brain Res 2001;894:336–339.CrossRefGoogle Scholar
Zhang, L., Bai, R., Liu, Y., Meng, L., Li, B., Wang, L., et al.The dose-dependent toxicological effects and potential perturbation on the neurotransmitter secretion in brain following intranasal instillation of copper nanoparticles. Nanotoxicology 2012;6:562–575.CrossRefGoogle ScholarPubMed
Okada, M., Mizuno, K., Okuyama, M., Kaneko, S.Magnesium ion augmentation of inhibitory effects of adenosine on dopamine release in the rat striatum. Psychiatry Clin Neurosci 1996;50:147–156.CrossRefGoogle ScholarPubMed
Buck, D.R., Mahoney, A.W., Hendricks, D.G.Effects of cerebral intraventricular magnesium injections and a low magnesium diet on nonspecific excitability level, audiogenic seizure susceptibility and serotonin. Pharmacol Biochem Behav 1979;10:487–491.CrossRefGoogle Scholar
Danysz, W., Parsons, C.G., Mobius, H.J., Stoffler, A., Quack, G.Neuroprotective and symptomatological action of memantine relevant for Alzheimer’s disease – a unified glutamatergic hypothesis on the mechanism of action. Neurotox Res 2000;2:85–97.CrossRefGoogle ScholarPubMed
Garcia-Colunga, J., Reyes-Haro, D., Godoy-Garcia, I.U., Miledi, R.Zinc modulation of serotonin uptake in the adult rat corpus callosum. J Neurosci Res 2005;80:145–149.CrossRefGoogle ScholarPubMed
Pifl, C., Wolf, A., Rebernik, P., Reither, H., Berger, M.L.Zinc regulates the dopamine transporter in a membrane potential and chloride dependent manner. Neuropharmacology 2009;56:531–540.CrossRefGoogle Scholar
Hollmann, M., Boulter, J., Maron, C., Beasley, L., Sullivan, J., Pecht, G., et al.Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 1993;10:943–954.CrossRefGoogle ScholarPubMed
Arinola, G., Idonije, B., Akinlade, K., Ihenyen, O.Essential trace metals and heavy metals in newly diagnosed schizophrenic patients and those on anti-psychotic medication. J Res Med Sci: Off J Isfahan Univ Med Sci 2010;15:245–249.Google ScholarPubMed
Matzen, T.A., Martin, R.L.Magnesium deficiency psychosis induced by cancer chemotherapy. Biol Psychiatry 1985;20:788–791.CrossRefGoogle ScholarPubMed
Nechifor, M., Vaideanu, C., Palamaru, I., Borza, C., Mindreci, I.The influence of some antipsychotics on erythrocyte magnesium and plasma magnesium, calcium, copper and zinc in patients with paranoid schizophrenia. J Am Coll Nutr 2004;23:549s–551s.CrossRefGoogle ScholarPubMed
Submit a response

Comments

No Comments have been published for this article.