Glucose Metabolism and Sex Hormones in Male Patients with
Medication-naïve First-episode Schizophrenia: A Large-scale
Cross-sectional Study

Meihong      Xiu; Meng      Hao; Cai      Liu; Maodi      Sun; Xiaoe      Lang

doi:10.2174/1570159X22666240212141602

Abstract

Background: Schizophrenia (SCZ) usually begins in early adult life. The underlying molecular mechanisms of SCZ remain unclear. There is evidence for the involvement of abnormalities in metabolic and endocrine systems in SCZ, even in drug-naïve first-episode schizophrenia patients (DNFES). However, the association between impaired regulation of glucose metabolism and sex hormones was not studied in SCZ. This study aimed to evaluate the interrelationship between sex hormones and high fasting glucose levels in male DNFES patients.

Methods: A total of 99 patients with SCZ were recruited, and fasting glucose, fasting insulin, the insulin resistance index (HOMA-IR), and sex hormones were measured.

Results: We found that some male patients with SCZ had abnormal levels in glucose metabolism parameters and gonadal hormones that were not within the normal range. Linear regression analysis adjusted for age, waist circumference, and body mass index showed that testosterone levels were negatively associated with fasting insulin in male patients (β = -0.21, t = -2.2, p = 0.03).

Conclusion: Our findings confirm the abnormalities in glucose metabolism parameters and gonadal hormones at the onset of the illness in male DNFES patients with SCZ. In addition, there was an interaction effect between abnormal glucose metabolism and sex hormones in male patients.

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[1]
Pedersen, C.B.; Mors, O.; Bertelsen, A.; Waltoft, B.L.; Agerbo, E.; McGrath, J.J.; Mortensen, P.B.; Eaton, W.W. A comprehensive nationwide study of the incidence rate and lifetime risk for treated mental disorders. JAMA Psychiatry,  2014, 71(5), 573-581.
 [http://dx.doi.org/10.1001/jamapsychiatry.2014.16] [PMID: 24806211]

[2]
Barnett, R. Schizophrenia. Lancet,  2018, 391(10121), 648.
 [http://dx.doi.org/10.1016/S0140-6736(18)30237-X] [PMID: 29617256]

[3]
Nguyen, K.D.; Amerio, A.; Aguglia, A.; Magnani, L.; Parise, A.; Conio, B.; Serafini, G.; Amore, M.; Costanza, A. Microglia and other cellular mediators of immunological dysfunction in schizophrenia: A narrative synthesis of clinical findings. Cells,  2023, 12(16), 2099.
 [http://dx.doi.org/10.3390/cells12162099] [PMID: 37626909]

[4]
Mitchell, A.J.; Vancampfort, D.; Sweers, K.; van Winkel, R.; Yu, W.; De Hert, M. Prevalence of metabolic syndrome and metabolic abnormalities in schizophrenia and related disorders: A systematic review and meta-analysis. Schizophr. Bull.,  2013, 39(2), 306-318.
 [http://dx.doi.org/10.1093/schbul/sbr148] [PMID: 22207632]

[5]
Correll, C.U.; Solmi, M.; Veronese, N.; Bortolato, B.; Rosson, S.; Santonastaso, P.; Thapa-Chhetri, N.; Fornaro, M.; Gallicchio, D.; Collantoni, E.; Pigato, G.; Favaro, A.; Monaco, F.; Kohler, C.; Vancampfort, D.; Ward, P.B.; Gaughran, F.; Carvalho, A.F.; Stubbs, B. Prevalence, incidence and mortality from cardiovascular disease in patients with pooled and specific severe mental illness: A large‐scale meta‐analysis of 3,211,768 patients and 113,383,368 controls. World Psychiatry,  2017, 16(2), 163-180.
 [http://dx.doi.org/10.1002/wps.20420] [PMID: 28498599]

[6]
Li, S.; Chen, D.; Xiu, M.; Li, J.; Zhang, X.Y. Diabetes mellitus, cognitive deficits and serum BDNF levels in chronic patients with schizophrenia: A case control study. J. Psychiatr. Res.,  2021, 134, 39-47.
 [http://dx.doi.org/10.1016/j.jpsychires.2020.12.035] [PMID: 33360223]

[7]
Li, S.; Gao, Y.; Lv, H.; Zhang, M.; Wang, L.; Jiang, R.; Xu, C.; Wang, X.; Gao, M.; He, Y.; Li, J.; Li, W.D. T4 and waist: Hip ratio as biomarkers of antipsychotic-induced weight gain in Han Chinese inpatients with schizophrenia. Psychoneuroendocrinology,  2018, 88, 54-60.
 [http://dx.doi.org/10.1016/j.psyneuen.2017.11.010] [PMID: 29175720]

[8]
Li, S.; Xu, C.; Tian, Y.; Wang, X.; Jiang, R.; Zhang, M.; Wang, L.; Yang, G.; Gao, Y.; Song, C.; He, Y.; Zhang, Y.; Li, J.; Li, W.D. TOX and ADIPOQ gene polymorphisms are associated with antipsychotic-induced weight gain in han chinese. Sci. Rep.,  2017, 7(1), 45203.
 [http://dx.doi.org/10.1038/srep45203] [PMID: 28327672]

[9]
Zhu, M.H.; Liu, Z.J.; Hu, Q.Y.; Yang, J.Y.; Jin, Y.; Zhu, N.; Huang, Y.; Shi, D.H.; Liu, M.J.; Tan, H.Y.; Zhao, L.; Lv, Q.Y.; Yi, Z.H.; Wu, F.C.; Li, Z.Z. Amisulpride augmentation therapy improves cognitive performance and psychopathology in clozapine resistant treatment refractory schizophrenia: A 12-week randomized, double-blind, placebo controlled trial. Mil. Med. Res.,  2022, 9(1), 59.
 [http://dx.doi.org/10.1186/s40779-022-00420-0] [PMID: 36253804]

[10]
Rajkumar, A.P.; Horsdal, H.T.; Wimberley, T.; Cohen, D.; Mors, O.; Børglum, A.D.; Gasse, C. Endogenous and antipsychotic related risks for diabetes mellitus in young people with schizophrenia: A danish population-based cohort study. Am. J. Psychiatry,  2017, 174(7), 686-694.
 [http://dx.doi.org/10.1176/appi.ajp.2016.16040442] [PMID: 28103712]

[11]
Chen, Y.Q.; Li, X.R.; Zhang, L.; Zhu, W.B.; Wu, Y.Q.; Guan, X.N.; Xiu, M.H.; Zhang, X.Y. Therapeutic response is associated with antipsychoticinduced weight gain in drug naive first episode patients with schizophrenia. J. Clin. Psychiatry,  2021, 82(3), 20m13469.
 [http://dx.doi.org/10.4088/JCP.20m13469] [PMID: 34004092]

[12]
Liu, H.; Yu, R.; Gao, Y.; Li, X.; Guan, X.; Thomas, K.; Xiu, M.; Zhang, X. Antioxidant enzymes and weight gain in drug-naive first-episode schizophrenia patients treated with risperidone for 12 weeks: A prospective longitudinal study. Curr. Neuropharmacol.,  2022, 20(9), 1774-1782.
 [http://dx.doi.org/10.2174/1570159X19666210920090547] [PMID: 34544343]

[13]
Liu, H.; Liu, H.; Jiang, S.; Su, L.; Lu, Y.; Chen, Z.; Li, X.; Li, X.; Wang, X.; Xiu, M.; Zhang, X. Sex-specific association between antioxidant defense system and therapeutic response to risperidone in schizophrenia: A prospective longitudinal study. Curr. Neuropharmacol.,  2022, 20(9), 1793-1803.
 [http://dx.doi.org/10.2174/1570159X19666211111123918] [PMID: 34766896]

[14]
Greenhalgh, A.M.; Gonzalez-Blanco, L.; Garcia-Rizo, C.; Fernandez-Egea, E.; Miller, B.; Arroyo, M.B.; Kirkpatrick, B. Meta-analysis of glucose tolerance, insulin, and insulin resistance in antipsychotic naïve patients with nonaffective psychosis. Schizophr. Res.,  2017, 179, 57-63.
 [http://dx.doi.org/10.1016/j.schres.2016.09.026] [PMID: 27743650]

[15]
Garcia-Rizo, C.; Fernandez-Egea, E.; Oliveira, C.; Meseguer, A.; Cabrera, B.; Mezquida, G.; Bioque, M.; Penades, R.; Parellada, E.; Bernardo, M.; Kirkpatrick, B. Metabolic syndrome or glucose challenge in first episode of psychosis? Eur. Psychiatry,  2017, 41(1), 42-46.
 [http://dx.doi.org/10.1016/j.eurpsy.2016.10.001] [PMID: 28049080]

[16]
Mizuki, Y.; Sakamoto, S.; Okahisa, Y.; Yada, Y.; Hashimoto, N.; Takaki, M.; Yamada, N. Mechanisms underlying the comorbidity of schizophrenia and type 2 diabetes mellitus. Int. J. Neuropsychopharmacol.,  2021, 24(5), 367-382.
 [http://dx.doi.org/10.1093/ijnp/pyaa097] [PMID: 33315097]

[17]
Pillinger, T.; Beck, K.; Gobjila, C.; Donocik, J.G.; Jauhar, S.; Howes, O.D. Impaired glucose homeostasis in first-episode schizophrenia. JAMA Psychiatry,  2017, 74(3), 261-269.
 [http://dx.doi.org/10.1001/jamapsychiatry.2016.3803] [PMID: 28097367]

[18]
Agarwal, S.M.; Caravaggio, F.; Costa-Dookhan, K.A.; Castellani, L.; Kowalchuk, C.; Asgariroozbehani, R.; Graff-Guerrero, A.; Hahn, M. Brain insulin action in schizophrenia: Something borrowed and something new. Neuropharmacology,  2020, 163, 107633.
 [http://dx.doi.org/10.1016/j.neuropharm.2019.05.010] [PMID: 31077731]

[19]
Bastemir, M.; Akin, F.; Emral, R.; Alkis, E. Impact of insulin sensitivity in relationship with prolactin and thyroid stimulating hormone. Exp. Clin. Endocrinol. Diabetes,  2007, 115(4), 257-260.
 [http://dx.doi.org/10.1055/s-2007-960492] [PMID: 17479443]

[20]
Li, J.; Rice, M.S.; Huang, T.; Hankinson, S.E.; Clevenger, C.V.; Hu, F.B.; Tworoger, S.S. Circulating prolactin concentrations and risk of type 2 diabetes in US women. Diabetologia,  2018, 61(12), 2549-2560.
 [http://dx.doi.org/10.1007/s00125-018-4733-9] [PMID: 30306190]

[21]
Wagner, R.; Heni, M.; Linder, K.; Ketterer, C.; Peter, A.; Böhm, A.; Hatziagelaki, E.; Stefan, N.; Staiger, H.; Häring, H.U.; Fritsche, A. Age-dependent association of serum prolactin with glycaemia and insulin sensitivity in humans. Acta Diabetol.,  2014, 51(1), 71-78.
 [http://dx.doi.org/10.1007/s00592-013-0493-7] [PMID: 23836327]

[22]
Le, T.N.; Celi, F.S.; Wickham, E.P., III Thyrotropin levels are associated with cardiometabolic risk factors in euthyroid adolescents. Thyroid,  2016, 26(10), 1441-1449.
 [http://dx.doi.org/10.1089/thy.2016.0055] [PMID: 27599541]

[23]
Lundbäck, V.; Ekbom, K.; Hagman, E.; Dahlman, I.; Marcus, C. Thyroid-stimulating hormone, degree of obesity, and metabolic risk markers in a cohort of swedish children with obesity. Horm. Res. Paediatr.,  2017, 88(2), 140-146.
 [http://dx.doi.org/10.1159/000475993] [PMID: 28614818]

[24]
Pintana, H.; Chattipakorn, N.; Chattipakorn, S. Testosterone deficiency, insulin-resistant obesity and cognitive function. Metab. Brain Dis.,  2015, 30(4), 853-876.
 [http://dx.doi.org/10.1007/s11011-015-9655-3] [PMID: 25703239]

[25]
Xia, F.; Xu, X.; Zhai, H.; Meng, Y.; Zhang, H.; Du, S.; Xu, H.; Wu, H.; Lu, Y. Castration-induced testosterone deficiency increases fasting glucose associated with hepatic and extra-hepatic insulin resistance in adult male rats. Reprod. Biol. Endocrinol.,  2013, 11(1), 106.
 [http://dx.doi.org/10.1186/1477-7827-11-106] [PMID: 24238614]

[26]
Gupte, A.A.; Pownall, H.J.; Hamilton, D.J. Estrogen: an emerging regulator of insulin action and mitochondrial function. J. Diabetes Res.,  2015, 2015, 1-9.
 [http://dx.doi.org/10.1155/2015/916585] [PMID: 25883987]

[27]
Brzezinski-Sinai, N.A.; Brzezinski, A. Schizophrenia and sex hormones: What is the link? Front. Psychiatry,  2020, 11, 693.
 [http://dx.doi.org/10.3389/fpsyt.2020.00693] [PMID: 32760302]

[28]
Gogos, A.; Ney, L.J.; Seymour, N.; Van Rheenen, T.E.; Felmingham, K.L. Sex differences in schizophrenia, bipolar disorder, and post‐traumatic stress disorder: Are gonadal hormones the link? Br. J. Pharmacol.,  2019, 176(21), 4119-4135.
 [http://dx.doi.org/10.1111/bph.14584] [PMID: 30658014]

[29]
Phillips, M.R.; Zhang, J.; Shi, Q.; Song, Z.; Ding, Z.; Pang, S.; Li, X.; Zhang, Y.; Wang, Z. Prevalence, treatment, and associated disability of mental disorders in four provinces in China during 2001–05: An epidemiological survey. Lancet,  2009, 373(9680), 2041-2053.
 [http://dx.doi.org/10.1016/S0140-6736(09)60660-7] [PMID: 19524780]

[30]
Lieberman, J.A.; Phillips, M.; Gu, H.; Stroup, S.; Zhang, P.; Kong, L.; Ji, Z.; Koch, G.; Hamer, R.M. Atypical and conventional antipsychotic drugs in treatment naive first episode schizophrenia: A 52-week randomized trial of clozapine vs. chlorpromazine. Neuropsychopharmacology,  2003, 28(5), 995-1003.
 [http://dx.doi.org/10.1038/sj.npp.1300157] [PMID: 12700715]

[31]
Zhang, X.; Yang, M.; Du, X.; Liao, W.; Chen, D.; Fan, F.; Xiu, M.; Jia, Q.; Ning, Y.; Huang, X.; Wu, F.; Soares, J.C.; Cao, B.; Wang, L.; Chen, H. Glucose disturbances, cognitive deficits and white matter abnormalities in first episode drug naive schizophrenia. Mol. Psychiatry,  2020, 25(12), 3220-3230.
 [http://dx.doi.org/10.1038/s41380-019-0478-1] [PMID: 31409883]

[32]
Xiu, M.; Fan, Y.; Liu, Q.; Chen, S.; Wu, F.; Zhang, X. Glucose metabolism, hippocampal subfields and cognition in first episode and never treated schizophrenia. Int. J. Clin. Health Psychol.,  2023, 23(4), 100402.
 [http://dx.doi.org/10.1016/j.ijchp.2023.100402] [PMID: 37663043]

[33]
Gao, Z.; Xiu, M.; Liu, J.; Wu, F.; Zhang, X.Y. Obesity, antioxidants and negative symptom improvement in first-episode schizophrenia patients treated with risperidone. Schizophrenia,  2023, 9(1), 17.
 [http://dx.doi.org/10.1038/s41537-023-00346-z] [PMID: 36949120]

[34]
Plum, L.; Schubert, M.; Brüning, J.C. The role of insulin receptor signaling in the brain. Trends Endocrinol. Metab.,  2005, 16(2), 59-65.
 [http://dx.doi.org/10.1016/j.tem.2005.01.008] [PMID: 15734146]

[35]
Tomasik, J.; Lago, S.G.; Vázquez-Bourgon, J.; Papiol, S.; Suárez-Pinilla, P.; Crespo-Facorro, B.; Bahn, S. Association of insulin resistance with schizophrenia polygenic risk score and response to antipsychotic treatment. JAMA Psychiatry,  2019, 76(8), 864-867.
 [http://dx.doi.org/10.1001/jamapsychiatry.2019.0304] [PMID: 30942838]

[36]
Freeman, L.R.; Haley-Zitlin, V.; Stevens, C.; Granholm, A.C. Diet-induced effects on neuronal and glial elements in the middle-aged rat hippocampus. Nutr. Neurosci.,  2011, 14(1), 32-44.
 [http://dx.doi.org/10.1179/174313211X12966635733358] [PMID: 21535919]

[37]
Zhao, Z.; Ksiezak-Reding, H.; Riggio, S.; Haroutunian, V.; Pasinetti, G.M. Insulin receptor deficits in schizophrenia and in cellular and animal models of insulin receptor dysfunction. Schizophr. Res.,  2006, 84(1), 1-14.
 [http://dx.doi.org/10.1016/j.schres.2006.02.009] [PMID: 16581231]

[38]
Emamian, E.S.; Hall, D.; Birnbaum, M.J.; Karayiorgou, M.; Gogos, J.A. Convergent evidence for impaired AKT1-GSK3β signaling in schizophrenia. Nat. Genet.,  2004, 36(2), 131-137.
 [http://dx.doi.org/10.1038/ng1296] [PMID: 14745448]

[39]
Kapogiannis, D.; Dobrowolny, H.; Tran, J.; Mustapic, M.; Frodl, T.; Meyer-Lotz, G.; Schiltz, K.; Schanze, D.; Rietschel, M.; Bernstein, H.G.; Steiner, J. Insulin-signaling abnormalities in drug-naïve first-episode schizophrenia: Transduction protein analyses in extracellular vesicles of putative neuronal origin. Eur. Psychiatry,  2019, 62, 124-129.
 [http://dx.doi.org/10.1016/j.eurpsy.2019.08.012] [PMID: 31590015]

[40]
Wijtenburg, S.A.; Kapogiannis, D.; Korenic, S.A.; Mullins, R.J.; Tran, J.; Gaston, F.E.; Chen, S.; Mustapic, M.; Hong, L.E.; Rowland, L.M. Brain insulin resistance and altered brain glucose are related to memory impairments in schizophrenia. Schizophr. Res.,  2019, 208, 324-330.
 [http://dx.doi.org/10.1016/j.schres.2019.01.031] [PMID: 30760413]

[41]
Fünfschilling, U.; Supplie, L.M.; Mahad, D.; Boretius, S.; Saab, A.S.; Edgar, J.; Brinkmann, B.G.; Kassmann, C.M.; Tzvetanova, I.D.; Möbius, W.; Diaz, F.; Meijer, D.; Suter, U.; Hamprecht, B.; Sereda, M.W.; Moraes, C.T.; Frahm, J.; Goebbels, S.; Nave, K.A. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature,  2012, 485(7399), 517-521.
 [http://dx.doi.org/10.1038/nature11007] [PMID: 22622581]

[42]
Steiner, J.; Bernstein, H.G.; Schiltz, K.; Müller, U.J.; Westphal, S.; Drexhage, H.A.; Bogerts, B. Immune system and glucose metabolism interaction in schizophrenia: A chicken–egg dilemma. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2014, 48, 287-294.
 [http://dx.doi.org/10.1016/j.pnpbp.2012.09.016] [PMID: 23085507]

[43]
Peters, A. The selfish brain: Competition for energy resources. Am. J. Hum. Biol.,  2011, 23(1), 29-34.
 [http://dx.doi.org/10.1002/ajhb.21106] [PMID: 21080380]

[44]
Veldhuis, J.D. Neuroendocrine mechanisms mediating awakening of the human gonadotropic axis in puberty. Pediatr. Nephrol.,  1996, 10(3), 304-317.
 [http://dx.doi.org/10.1007/BF00866767] [PMID: 8792395]

[45]
Hwang, W.J.; Lee, T.Y.; Kim, N.S.; Kwon, J.S. The role of estrogen receptors and their signaling across psychiatric disorders. Int. J. Mol. Sci.,  2020, 22(1), 373.
 [http://dx.doi.org/10.3390/ijms22010373] [PMID: 33396472]

[46]
Gonçalves, V.F.; Cuperfain, A.B.; Kennedy, J.L. Sex differences in schizophrenia: estrogen and mitochondria. Neuropsychopharmacology,  2019, 44(1), 216-217.
 [http://dx.doi.org/10.1038/s41386-018-0228-0] [PMID: 30294000]

[47]
Sinclair, D.; Purves-Tyson, T.D.; Allen, K.M.; Weickert, C.S. Impacts of stress and sex hormones on dopamine neurotransmission in the adolescent brain. Psychopharmacology,  2014, 231(8), 1581-1599.
 [http://dx.doi.org/10.1007/s00213-013-3415-z] [PMID: 24481565]

[48]
Cosgrove, K.P.; Mazure, C.M.; Staley, J.K. Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol. Psychiatry,  2007, 62(8), 847-855.
 [http://dx.doi.org/10.1016/j.biopsych.2007.03.001] [PMID: 17544382]

[49]
Kulkarni, J.; Gavrilidis, E.; Worsley, R.; Hayes, E. Role of estrogen treatment in the management of schizophrenia. CNS Drugs,  2012, 26(7), 549-557.
 [http://dx.doi.org/10.2165/11630660-000000000-00000] [PMID: 22626057]

[50]
Brandt, N.; Fester, L.; Rune, G.M. Neural sex steroids and hippocampal synaptic plasticity. Vitam. Horm.,  2020, 114, 125-143.
 [http://dx.doi.org/10.1016/bs.vh.2020.06.001] [PMID: 32723541]

[51]
Rocks, D.; Kundakovic, M.J.J.o.N. Hippocampus‐based behavioral, structural, and molecular dynamics across the estrous cycle. J. Neuroendocrinol.,  2023, 35(2), e13216.
 [http://dx.doi.org/10.1111/jne.13216]

[52]
Pratchayasakul, W.; Sa-nguanmoo, P.; Sivasinprasasn, S.; Pintana, H.; Tawinvisan, R.; Sripetchwandee, J.; Kumfu, S.; Chattipakorn, N.; Chattipakorn, S.C. Obesity accelerates cognitive decline by aggravating mitochondrial dysfunction, insulin resistance and synaptic dysfunction under estrogen-deprived conditions. Horm. Behav.,  2015, 72, 68-77.
 [http://dx.doi.org/10.1016/j.yhbeh.2015.04.023] [PMID: 25989597]

[53]
Luo, M.; Zeng, Q.; Jiang, K.; Zhao, Y.; Long, Z.; Du, Y.; Wang, K.; He, G. Estrogen deficiency exacerbates learning and memory deficits associated with glucose metabolism disorder in APP/PS1 double transgenic female mice. Genes Dis.,  2022, 9(5), 1315-1331.
 [http://dx.doi.org/10.1016/j.gendis.2021.01.007] [PMID: 35873026]

[54]
Redman, B.; Kitchen, C.; Johnson, K.W.; Bezwada, P.; Kelly, D.L. Levels of prolactin and testosterone and associated sexual dysfunction and breast abnormalities in men with schizophrenia treated with antipsychotic medications. J. Psychiatr. Res.,  2021, 143, 50-53.
 [http://dx.doi.org/10.1016/j.jpsychires.2021.08.022] [PMID: 34450525]

[55]
Mauvais-Jarvis, F. Role of sex steroids in β cell function, growth, and survival. Trends Endocrinol. Metab.,  2016, 27(12), 844-855.
 [http://dx.doi.org/10.1016/j.tem.2016.08.008] [PMID: 27640750]

[56]
Filippi, S.; Vignozzi, L.; Morelli, A.; Chavalmane, A.K.; Sarchielli, E.; Fibbi, B.; Saad, F.; Sandner, P.; Ruggiano, P.; Vannelli, G.B.; Mannucci, E.; Maggi, M. Testosterone partially ameliorates metabolic profile and erectile responsiveness to PDE5 inhibitors in an animal model of male metabolic syndrome. J. Sex. Med.,  2009, 6(12), 3274-3288.
 [http://dx.doi.org/10.1111/j.1743-6109.2009.01467.x] [PMID: 19732305]

[57]
Ribeiro, D.L.; Pinto, M.E.; Rafacho, A.; Bosqueiro, J.R.; Maeda, S.Y.; Anselmo-Franci, J.A.; Taboga, S.R.; Góes, R.M. High-fat diet obesity associated with insulin resistance increases cell proliferation, estrogen receptor, and PI3K proteins in rat ventral prostate. J. Androl.,  2012, 33(5), 854-865.
 [http://dx.doi.org/10.2164/jandrol.111.016089] [PMID: 22441765]

[58]
Vignozzi, L.; Morelli, A.; Sarchielli, E.; Comeglio, P.; Filippi, S.; Cellai, I.; Maneschi, E.; Serni, S.; Gacci, M.; Carini, M.; Piccinni, M.P.; Saad, F.; Adorini, L.; Vannelli, G.B.; Maggi, M. Testosterone protects from metabolic syndrome-associated prostate inflammation: An experimental study in rabbit. J. Endocrinol.,  2012, 212(1), 71-84.
 [http://dx.doi.org/10.1530/JOE-11-0289] [PMID: 22010203]

[59]
Vigueras-Villaseñor, R.M.; Rojas-Castañeda, J.C.; Chávez-Saldaña, M.; Gutiérrez-Pérez, O.; García-Cruz, M.E.; Cuevas-Alpuche, O.; Reyes-Romero, M.M.; Zambrano, E. Alterations in the spermatic function generated by obesity in rats. Acta Histochem.,  2011, 113(2), 214-220.
 [http://dx.doi.org/10.1016/j.acthis.2009.10.004] [PMID: 20149418]

[60]
Fanelli, G.; Gevi, F.; Belardo, A.; Zolla, L. Metabolic patterns in insulin-sensitive male hypogonadism. Cell Death Dis.,  2018, 9(6), 653.
 [http://dx.doi.org/10.1038/s41419-018-0588-8] [PMID: 29844353]

[61]
Souteiro, P.; Belo, S.; Oliveira, S.C.; Neves, J.S.; Magalhães, D.; Pedro, J.; Bettencourt-Silva, R.; Costa, M.M.; Varela, A.; Queirós, J.; Freitas, P.; Carvalho, D. Insulin resistance and sex hormone-binding globulin are independently correlated with low free testosterone levels in obese males. Andrologia,  2018, 50(7), e13035.
 [http://dx.doi.org/10.1111/and.13035] [PMID: 29744905]

[62]
Melcangi, R.C.; Panzica, G.; Garcia-Segura, L.M. Neuroactive steroids: focus on human brain. Neuroscience,  2011, 191, 1-5.
 [http://dx.doi.org/10.1016/j.neuroscience.2011.06.024] [PMID: 21704130]

[63]
Reddy, D.S. Neurosteroids.   Prog. Brain Res.,  2010, 186, 113-137.
 [http://dx.doi.org/10.1016/B978-0-444-53630-3.00008-7] [PMID: 21094889]

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Current Neuropharmacology

Glucose Metabolism and Sex Hormones in Male Patients with Medication-naïve First-episode Schizophrenia: A Large-scale Cross-sectional Study

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