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Low cholesterol levels in children predict impulsivity in young adulthood

Published online by Cambridge University Press:  02 December 2019

Katrin Tomson-Johanson
Affiliation:
Division of Neuropsychopharmacology, Department of Psychology, University of Tartu, Tartu, Estonia Department of Family Medicine and Public Health, University of Tartu, Tartu, Estonia
Tanel Kaart
Affiliation:
Chair of Animal Breeding and Biotechnology, Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Tartu, Estonia
Raul-Allan Kiivet
Affiliation:
Department of Family Medicine and Public Health, University of Tartu, Tartu, Estonia
Toomas Veidebaum
Affiliation:
National Institute for Health Development, Tallinn, Estonia
Jaanus Harro*
Affiliation:
Division of Neuropsychopharmacology, Department of Psychology, University of Tartu, Tartu, Estonia
*
Author for correspondence: Jaanus Harro, Email: [email protected]

Abstract

Objective:

Severe behavioural issues such as impulsive action and suicide have since long been associated with low levels of cholesterol. While it is known that cholesterol plays a role in neural development and hence low levels of serum lipids could have long-term effects on behaviour, no longitudinal studies showed the association of serum lipids levels with impulsivity. We aimed to examine the prognostic properties of serum lipid levels during childhood and adolescence on measures of impulsivity during early adulthood in a representative birth cohort sample.

Methods:

We have investigated whether serum lipid levels measured at 9, 15, 18 and 25 years of age have an association with impulsivity in 25 years old young adults. This analysis was based on data of the birth cohort representative samples of the Estonian Children Personality Behaviour and Health Study (original n = 1238). Impulsivity was self-reported with the Adaptive and Maladaptive Impulsivity Scale.

Results:

Total and low-density lipoprotein (LDL) cholesterol measured in boys aged 9, 15 and 18 years predicted disinhibition and thoughtlessness in 25-year-old young adults. High scores of disinhibition were associated with low total and LDL cholesterol levels in males but, while less consistently, with high total and LDL cholesterol levels in females. Cross-sectional analysis did not result in systematic outcomes.

Conclusions:

Serum lipid levels could have an impact on the development of Maladaptive Impulsivity starting from an early age. This effect of cholesterol continues throughout adolescence into young adulthood.

Type
Original Article
Copyright
© Scandinavian College of Neuropsychopharmacology 2019

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References

Apter, A, Laufer, N, Barsever, M, Hareven, D, Ofek, H and Weizman, A. (1999) Serum Cholesterol suicidal tendencies impulsivity aggression and depression in adolescent psychiatric inpatients. Biological Psychiatry 46 (4), 532541.CrossRefGoogle ScholarPubMed
Asellus, P, Nordström, P, Nordström, AL and Jokinen, J. (2014) Cholesterol and the “Cycle of Violence” in attempted suicide. Psychiatry Research 215 (3), 646650.CrossRefGoogle Scholar
Balder, JW, Lansberg, PJ, Hof, MH, Wiegman, A, Hutten, BA and Kuivenhoven, JA. (2018) Pediatric lipid reference values in the general population: the Dutch lifelines cohort study. Journal of Clinical Lipidology 12 (5), 12081216.CrossRefGoogle ScholarPubMed
Barratt, ES, Stanford, MS, Dowdy, L, Liebman, MJ and Kent, TA. (1999) Impulsive and premeditated aggression: a factor analysis of self-reported acts. Psychiatry Research 86 (2), 163173.CrossRefGoogle ScholarPubMed
Bartoli, F, Crocamo, C, Dakanalis, A, Riboldi, I, Miotto, A, Brosio, E and Carrà, G. (2017) Association between total serum cholesterol and suicide attempts in subjects with major depressive disorder: exploring the role of clinical and biochemical confounding factors. Clinical Biochemistry 50 (6), 274278.CrossRefGoogle ScholarPubMed
Björk, K, Sjögren, B and Svenningsson, P. (2010) Regulation of serotonin receptor function in the nervous system by lipid rafts and adaptor proteins. Experimental Cell Research 316 (8), 13511356.CrossRefGoogle ScholarPubMed
Björkhem, I, Lutjohann, D, Diczfalusy, U, Stahle, L, Ahlborg, G and Wahren, J. (1998) Cholesterol homeostasis in human brain: turnover of 24S-hydroxycholesterol and evidence for a cerebral origin of most of this oxysterol in the circulation. Journal of Lipid Research 39 (8), 15941600.Google ScholarPubMed
Bruses, JL, Chauvet, N and Rutishauser, U. (2001) Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 21 (2), 504512.CrossRefGoogle ScholarPubMed
Casey, B, Getz, S and Galvan, A. (2008) The adolecent brain. Developmental Review 28 (1), 6277.CrossRefGoogle Scholar
Corruble, E, Damy, C and Guelfi, JD. (1999) Impulsivity: a relevant dimension in depression regarding suicide attempts? Journal of Affective Disorders 53 (3), 211215.CrossRefGoogle ScholarPubMed
Daray, FM, Mann, JJ and Sublette, ME. (2018) How lipids may affect risk for suicidal behavior. Journal of Psychiatric Research 104, 1623.CrossRefGoogle ScholarPubMed
Dickman, SJ. (1990) Functional and dysfunctional impulsivity: personality and cognitive correlates. Journal of Personality and Social Psychology 58 (1), 95102.CrossRefGoogle ScholarPubMed
Dougherty, DM, Bjork, JM, Marsh, DM and Moeller, FG. (1999) Influence of trait hostility on tryptophan depletion-induced laboratory aggression. Psychiatry Research 88 (3), 227232.CrossRefGoogle ScholarPubMed
Eensoo, D, Paaver, M, Pulver, A, Harro, M and Harro, J. (2004) Low platelet MAO activity associated with high dysfunctional impulsivity and antisocial behavior: evidence from drunk drivers. Psychopharmacology 172 (3), 356358.CrossRefGoogle ScholarPubMed
Eensoo, D, Paaver, M, Vaht, M, Loit, H-M and Harro, J. (2018) Risky driving and the persistent effect of a randomized intervention focusing on impulsivity: the role of the serotonin transporter promoter polymorphism. Accident; Analysis and Prevention 113, 1924.CrossRefGoogle ScholarPubMed
Engelberg, H. (1992) Low serum cholesterol and suicide. Lancet 339 (8795), 727729.CrossRefGoogle ScholarPubMed
Eriksen, BMS, Bjørkly, S, Lockertsen, Ø, Færden, A and Roaldset, JO. (2017) Low cholesterol level as a risk marker of inpatient and post-discharge violence in acute psychiatry – A prospective study with a focus on gender differences. Psychiatry Research 255, 17.CrossRefGoogle ScholarPubMed
Favaro, A and Santonastaso, P. (1997) Suicidality in eating disorders: clinical and psychological correlates. Acta Psychiatrica Scandinavica 95 (6), 508514.CrossRefGoogle ScholarPubMed
Fowkes, FG, Leng, GC, Donnan, PT, Deary, IJ, Riemersma, RA and Housley, E. (1992) Serum cholesterol triglycerides and aggression in the general population. Lancet 340 (8826), 995998.CrossRefGoogle ScholarPubMed
Golier, JA, Marzuk, PM, Leon, AC, Weiner, C and Tardiff, K. (1995) Low serum cholesterol level and attempted suicide. The American Journal of Psychiatry 152 (3), 419423.Google ScholarPubMed
Goritz, C, Mauch, DH and Pfrieger, FW. (2005) Multiple mechanisms mediate cholesterol-induced synaptogenesis in a CNS neuron. Molecular and Cellular Neurosciences 29 (2), 190201.CrossRefGoogle Scholar
Harro, J and Oreland, L. (2016) The role of MAO in personality and drug use. Progress in Neuro-Psychopharmacology and Biological Psychiatry 69, 101111.CrossRefGoogle ScholarPubMed
Harro, M, Eensoo, D, Kiive, E, Merenakk, L, Alep, J, Oreland, L and Harro, J. (2001) Platelet monoamine oxidase in healthy 9- and 15-years old children: the effect of gender smoking and puberty. Progress in Neuro-Psychopharmacology and Biological Psychiatry 25 (8), 14971511.CrossRefGoogle ScholarPubMed
Hillbrand, M, Waite, B, Miller, DS, Spitz, RT and Lingswiler, VM. (2000) Serum cholesterol concentrations and mood states in violent psychiatric patients: an experience sampling study. Journal of Behavioral Medicine 23 (6), 519529.CrossRefGoogle ScholarPubMed
Jovanovic, H, Lundberg, J, Karlsson, P, Cerin, Å, Saijo, T, Varrone, A and Nordström, AL. (2008) Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. NeuroImage 39 (3), 14081419.CrossRefGoogle ScholarPubMed
Kaplan, JR, Muldoon, MF, Manuck, SB and Mann, JJ. (1997) Assessing the observed relationship between low cholesterol and violence-related mortality Implications for suicide risk. Annals of the New York Academy of Sciences 836, 5780.CrossRefGoogle ScholarPubMed
Kavoor, AR, Mitra, S, Kumar, S, Sisodia, AK and Jain, R. (2017) Lipids aggression suicidality and impulsivity in drug-naïve/drug-free patients of schizophrenia. Asian Journal of Psychiatry 27, 129136.CrossRefGoogle ScholarPubMed
Kiive, E, Kurrikoff, T, Maestu, J and Harro, J. (2010) Effect of alpha2A-adrenoceptor C-1291G genotype and maltreatment on hyperactivity and inattention in adolescents. Progress in Neuro-Psychopharmacology and Biological Psychiatry 34 (1), 219224.CrossRefGoogle ScholarPubMed
Kotting, WF, Bubenzer, S, Helmbold, K, Eisert, A, Gaber, TJ and Zepf, FD. (2013) Effects of tryptophan depletion on reactive aggression and aggressive decision-making in young people with ADHD. Acta Psychiatrica Scandinavica 128 (2), 114123.CrossRefGoogle Scholar
Kraav, SL, Tolmunen, T, Kärkkäinen, O, Ruusunen, A, Viinamäki, H, Mäntyselkä, P, Koivumaa-Honkanen, H, Valkonen-Korhonen, M, Honkalampi, K, Herzig, KH and Lehto, SM. (2019) Decreased serum total cholesterol is associated with a history of childhood physical violence in depressed outpatients. Psychiatry Research 272, 326333.CrossRefGoogle ScholarPubMed
Laas, K, Eensoo, D, Paaver, M, Lesch, KP, Reif, A and Harro, J. (2015a) Further evidence for the association of the NPSR1 gene A/T polymorphism (Asn107Ile) with impulsivity and hyperactivity. Journal of Psychopharmacology 29 (8), 878–83.CrossRefGoogle Scholar
Laas, K, Kiive, E, Mäestu, J, Vaht, M, Veidebaum, T and Harro, J. (2017) Nice guys: homozygocity for the TPH2 -703G/T (rs4570625) minor allele promotes low aggressiveness and low anxiety. Journal of Affective Disorders. 215, 230236.CrossRefGoogle ScholarPubMed
Laas, K, Reif, A, Akkermann, K, Kiive, E, Domschke, K, Lesch, KP, Veidebaum, T and Harro, J. (2015b) Neuropeptide S receptor gene variant and environment: contribution to alcohol use disorders and alcohol consumption. Addiction Biology 20 (3), 605–16.CrossRefGoogle ScholarPubMed
Laas, K, Reif, A, Herterich, S, Eensoo, D, Lesch, KP and Harro, J. (2010) The effect of a functional NOS1 promoter polymorphism on impulsivity is moderated by platelet MAO activity. Psychopharmacology 209 (3), 255261.CrossRefGoogle ScholarPubMed
Lindberg, G, Rastam, L, Gullberg, B and Eklund, GA. (1992) Low serum cholesterol concentration and short term mortality from injuries in men and women. BMJ 305 (6848), 277279.CrossRefGoogle ScholarPubMed
Luht, K, Tokko, T, Eensoo, D, Vaht, M and Harro, J. (2019) Efficacy of intervention at traffic schools reducing impulsive action and association with candidate gene variants. Acta Neuropsychiatrica 31 (3), 159166.CrossRefGoogle ScholarPubMed
Markovitz, JH, Smith, D, Raczynski, JM, Oberman, A, Williams, OD, Knox, S and Jr Jacobs, DR. (1997) Lack of relations of hostility negative affect and high-risk behavior with low plasma lipid levels in the Coronary Artery Risk Development in Young Adults Study. Archives of Internal Medicine 157, 19531959.CrossRefGoogle ScholarPubMed
Matsuda, A, Nagao, K, Matsuo, M, Kioka, N and Ueda, K. (2013) 24(S)-hydroxycholesterol is actively eliminated from neuronal cells by ABCA1. Journal of Neurochemistry 126, 93101.CrossRefGoogle ScholarPubMed
Mauch, DH, Nagler, K, Schumacher, S, Goritz, C, Muller, EC, Otto, A and Pfrieger, FW. (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294 (5545), 13541357.CrossRefGoogle ScholarPubMed
Mensi, R, Messaoud, A, Mhallah, A, Azizi, I, Salah, WH, Douki, W and Gaha, L. (2016) The association between altered lipid profile and suicide attempt among Tunisian patients with schizophrenia. Annals of General Psychiatry 15 (1), 19.CrossRefGoogle ScholarPubMed
Messaoud, A, Mensi, R, Mrad, A, Mhalla, A, Azizi, I, Amemou, B and Gaha, L. (2017) Is low total cholesterol levels associated with suicide attempt in depressive patients? Annals of General Psychiatry 16 (1), 18.CrossRefGoogle ScholarPubMed
Miyazaki, K, Miyazaki, KW and Doya, K. (2012) The role of serotonin in the regulation of patience and impulsivity. Molecular Neurobiology 45 (2), 213224.CrossRefGoogle ScholarPubMed
Muldoon, MF, Manuck, SB and Matthews, KA. (1990) Lowering cholesterol concentrations and mortality: a quantitative review of primary prevention trials. BMJ 301 (6747), 309314.CrossRefGoogle ScholarPubMed
Naiberg, MR, Newton, DF, Collins, JE, Bowie, CR and Goldstein, BI (2016) Impulsivity is associated with blood pressure and waist circumference among adolescents with bipolar disorder. Journal of Psychiatric Research 83, 230239.CrossRefGoogle ScholarPubMed
National Cholesterol Education Program (NCEP) (1992) Highlights of the report of the expert panel on blood cholesterol levels in children and adolescents. Pediatrics 89 (3), 495501.Google Scholar
Nishizawa, S, Benkelfat, C, Young, SN, Leyton, M, Mzengeza, S, de Montigny, C and Diksic, M. (1997) Differences between males and females in rates of serotonin synthesis in human brain. Proceedings of the National Academy of Sciences of the United States of America 94 (10), 53085313.CrossRefGoogle ScholarPubMed
Ohvo-Rekila, H, Ramstedt, B, Leppimaki, P and Slotte, JP. (2002) Cholesterol interactions with phospholipids in membranes. Progress in Lipid Research 41 (1), 6697.CrossRefGoogle ScholarPubMed
Paaver, M, Eensoo, D, Pulver, A and Harro, J. (2006) Adaptive and maladaptive impulsivity, platelet monoamine oxidase (MAO) activity and risk-admitting in different types of risky drivers. Psychopharmacology 186 (1), 3240.CrossRefGoogle ScholarPubMed
Paaver, M, Kurrikoff, T, Nordquist, N, Oreland, L and Harro, J. (2008) The effect of 5-HTT gene promoter polymorphism on impulsivity depends on family relations in girls. Progress in Neuro-Psychopharmacology and Biological Psychiatry 32 (5), 12631268.CrossRefGoogle ScholarPubMed
Papakostas, GI, Öngür, D, Iosifescu, DV, Mischoulon, D and Fava, M. (2004) Cholesterol in mood and anxiety disorders: review of the literature and new hypotheses. European Neuropsychopharmacology 14, 135142.CrossRefGoogle ScholarPubMed
Plana, T, Gracia, R, Méndez, I, Pintor, L, Lazaro, L and Castro-Fornieles, J. (2010) Total serum cholesterol levels and suicide attempts in child and adolescent psychiatric inpatients. European Child and Adolescent Psychiatry 19 (7), 615619.CrossRefGoogle ScholarPubMed
Pozzi, F, Troisi, A, Cerilli, M, Autore, AM, Lo Castro, L and Ribatti, D. (2003) Serum cholesterol and impulsivity in a large sample of healthy young men. British Medical Journal 120 (3), 239245.Google Scholar
Pucadyil, TJ and Chattopadhyay, A. (2004) Cholesterol modulates ligand binding and G-protein coupling to serotonin1A receptors from bovine hippocampus. Biochimica et Biophysica Acta - Biomembranes 1663 (1–2), 188200.CrossRefGoogle Scholar
Repo-Tiihonen, E, Halonen, P, Tiihonen, J and Virkkunen, M. (2002) Total serum cholesterol level violent criminal offences suicidal behavior mortality and the appearance of conduct disorder in Finnish male criminal offenders with antisocial personality disorder. European Archives of Psychiatry and Clinical Neuroscience 252 (1), 811.CrossRefGoogle ScholarPubMed
Roaldset, JO, Bakken, AM and Bjørkly, S. (2011) A prospective study of lipids and serotonin as risk markers of violence and self-harm in acute psychiatric patients. Psychiatry Research 186 (2–3), 293299.CrossRefGoogle ScholarPubMed
Romer, D (2012) Adolescent risk taking impulsivity and brain development: implications for prevention. Developmental Psychobiology 52 (3), 263276.Google Scholar
Roy, A, Laas, K, Kurrikoff, T, Reif, A, Veidebaum, T, Lesch, K-P and Harro, J. (2018) Family environment interacts with CRHR1 rs17689918 to predict mental health and behavioral outcomes. Progress in Neuro-Psychopharmacology and Biological Psychiatry 86, 4551.CrossRefGoogle ScholarPubMed
Sahebzamani, FM, D’Aoust, RF, Friedrich, D, Aiyer, AN, Reis, SE and Kip, KE. (2013) Relationship among low cholesterol levels depressive symptoms aggression hostility and cynicism. Journal of Clinical Lipidology 7 (3), 208216.CrossRefGoogle ScholarPubMed
Scanlon, SM, Williams, DC and Schloss, P. (2001) Membrane cholesterol modulates serotonin transporter activity. Biochemistry 40 (35), 1050710513.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E and Dunbar, GC. (1998) The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. The Journal of Clinical Psychiatry 20, 2257.Google Scholar
Shlik, J, Aluoja, A and Kihl, E. (1999) MINI 5.0.0. Mini rahvusvaheline neuropsühhiaatriline intervjuu DSM –IV. Estonian version of MINI international neuropsychiatric interview.Google Scholar
Siegman, AW, Malkin, AR, Boyle, S, Vaitkus, M, Barko, W and Franco, E. (2002) Anger and plasma lipid lipoprotein and glucose levels in healthy women: the mediating role of physical fitness. Journal of Behavioral Medicine 25 (1), 116.CrossRefGoogle ScholarPubMed
Simons, K and Vaz, WL. (2005) Model systems, lipid rafts, and cell membranes. Annual Review of Biophysics and Biomolecular Structure 33, 269–265.CrossRefGoogle Scholar
Sjöegren, B, Hamblin, MW and Svenningsson, P. (2006) Cholesterol depletion reduces serotonin binding and signaling via human 5-HT7(a) receptors. European Journal of Pharmacology 552 (1–3), 110.CrossRefGoogle Scholar
Soloff, PH, Chiappetta, L, Mason, NS, Becker, C and Price, JC. (2014) Effects of serotonin-2A receptor binding and gender on personality traits and suicidal behavior in borderline personality disorder. Psychiatry Research 222 (3), 140148.CrossRefGoogle ScholarPubMed
Sooksawate, T and Simmonds, MA. (2001) Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology 40 (2), 178184.CrossRefGoogle ScholarPubMed
Stavnsbo, M, Resaland, GK, Anderssen, SA, Steene-Johannessen, J, Domazet, SL, Skrede, T, Sardinha, LB, Kriemler, S, Ekelund, U, Andersen, LB and Aadland, E. (2018) Reference values for cardiometabolic risk scores in children and adolescents: suggesting a common standard. Atherosclerosis 278, 299306.CrossRefGoogle ScholarPubMed
Steegmans, PH, Fekkes, D, Hoes, AW, Bak, AA, van der Does, E and Grobbee, DE. (1996) Low serum cholesterol concentration and serotonin metabolism in men. British Medical Journal 312 (7025), 221.CrossRefGoogle ScholarPubMed
Steinberg, L. (2008) Neuroscience perspective on adolescent risk taking. Developmental Review 28 (1), 127.CrossRefGoogle ScholarPubMed
Strand, MF, Fredriksen, PM, Hjelle, OP and Lindberg, M. (2018) Reference intervals for serum lipids and prevalence of dyslipidaemia in 6-12-year-old children: the Health Oriented Pedagogical Project (HOPP). Scandinavian Journal of Public Health 46, 2127.CrossRefGoogle Scholar
Suzuki, T, Ito, J, Takagi, H, Saitoh, F, Nawa, H and Shimizu, H. (2001) Biochemical evidence for localization of AMPA-type glutamate receptor subunits in the dendritic raft. Brain Research Molecular Brain Research 89 (1–2), 2028.CrossRefGoogle ScholarPubMed
Svensson, T, Inoue, M, Sawada, N, Charvat, H, Mimura, M, Tsugane, S and Sato, Y. (2017) High serum total cholesterol is associated with suicide mortality in Japanese women. Acta Psychiatrica Scandinavica 136 (3), 259268.CrossRefGoogle ScholarPubMed
Terao, T, Nakamura, J, Yoshimura, R, Ohmori, O, Takahashi, N, Kojima, H and Okuno, T. (2000) Relationship between serum cholesterol levels and meta-chlorophenylpiperazine-induced cortisol responses in healthy men and women. Psychiatry Research 96 (2), 167173.CrossRefGoogle ScholarPubMed
Tokko, T, Eensoo, D, Vaht, M, Lesch, K-P, Reif, A and Harro, J. (2019) Relapse of drunk driving and association with traffic accidents alcohol-related problems and biomarkers of impulsivity. Acta Neuropsychiatrica 31 (2), 8492.CrossRefGoogle ScholarPubMed
Tomson, K, Merenäkk, L, Loit, H-M, Mäestu, J and Harro, J. (2011) The relationship between serotonin transporter gene promoter polymorphism and serum lipid levels at young age in a longitudinal population-representative study. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35 (8), 18571862.CrossRefGoogle Scholar
Tomson, K, Vaht, M, Laas, K, Veidebaum, T and Harro, J. (2016) Effect of a human serotonin 5-HT2A receptor gene polymorphism on impulsivity: dependence on cholesterol levels. Journal of Affective Disorders 206, 2330.CrossRefGoogle ScholarPubMed
Tomson-Johanson, K and Harro, J. (2018) Low cholesterol impulsivity and violence revisited. Current Opinion in Endocrinology Diabetes and Obesity 25 (2), 103107.CrossRefGoogle ScholarPubMed
Troisi, A. (2011) Low cholesterol is a risk factor for attentional impulsivity in patients with mood symptoms. Psychiatry Research 188 (1), 8387.CrossRefGoogle ScholarPubMed
Vevera, J, Žukov, I, Morcinek, T and Papežová, H. (2003) Cholesterol concentrations in violent and non-violent women suicide attempters. European Psychiatry 18, 2327.CrossRefGoogle ScholarPubMed
Walderhaug, E, Herman, AI, Magnusson, A, Morgan, MJ and Landro, NI. (2010) The short (S) allele of the serotonin transporter polymorphism and acute tryptophan depletion both increase impulsivity in men. Neuroscience Letters 473 (3), 208211.CrossRefGoogle ScholarPubMed
Walderhaug, E, Magnusson, A, Neumeister, A, Lappalainen, J, Lunde, H, Refsum, H and Landro, NI. (2007) Interactive effects of sex and 5-HTTLPR on mood and impulsivity during tryptophan depletion in healthy people. Biological Psychiatry 62 (6), 593599.CrossRefGoogle ScholarPubMed
Winocour, PH, Ishola, M and Durrington, PN. (1989) Validation of the Friedewald formula for the measurement of low density lipoprotein cholesterol in insulin-dependent diabetes mellitus. Clinica Chimica Acta 179 (1), 7983.CrossRefGoogle ScholarPubMed
Wu, S, Ding, Y, Wu, F, Xie, G, Hou, J and Mao, P. (2015) Serum lipid levels and suicidality: a meta-analysis of 65 epidemiological studies. Journal of Psychiatry and Neuroscience 41 (1), 5669.CrossRefGoogle Scholar
Zhang, J and Liu, Q. (2015) Cholesterol metabolism and homeostasis in the brain. Protein Cell 6 (4), 254264.CrossRefGoogle Scholar
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