Glucose Metabolism and Sex Hormones in Male Patients with Medication-naïve First-episode Schizophrenia: A Large-scale Cross-sectional Study
- Authors: Xiu M.1, Hao M.2, Liu C.3, Sun M.4, Lang X.3
-
Affiliations:
- Beijing Huilongguan Hospital, Peking University HuiLongGuan Clinical Medical School
- Department of Psychiatry, First Hospital of Shanxi Medical University,
- Department of Psychiatry, First Hospital of Shanxi Medical University
- , North University of China
- Issue: Vol 22, No 13 (2024)
- Pages: 2263-2270
- Section: Neurology
- URL: https://rjpbr.com/1570-159X/article/view/644513
- DOI: https://doi.org/10.2174/1570159X22666240212141602
- ID: 644513
Cite item
Full Text
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.
About the authors
Meihong Xiu
Beijing Huilongguan Hospital, Peking University HuiLongGuan Clinical Medical School
Email: info@benthamscience.net
Meng Hao
Department of Psychiatry, First Hospital of Shanxi Medical University,
Email: info@benthamscience.net
Cai Liu
Department of Psychiatry, First Hospital of Shanxi Medical University
Email: info@benthamscience.net
Maodi Sun
, North University of China
Email: info@benthamscience.net
Xiaoe Lang
Department of Psychiatry, First Hospital of Shanxi Medical University
Author for correspondence.
Email: info@benthamscience.net
References
- 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. doi: 10.1001/jamapsychiatry.2014.16 PMID: 24806211
- Barnett, R. Schizophrenia. Lancet, 2018, 391(10121), 648. doi: 10.1016/S0140-6736(18)30237-X PMID: 29617256
- 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. doi: 10.3390/cells12162099 PMID: 37626909
- 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. doi: 10.1093/schbul/sbr148 PMID: 22207632
- 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. doi: 10.1002/wps.20420 PMID: 28498599
- 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. doi: 10.1016/j.jpsychires.2020.12.035 PMID: 33360223
- 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. doi: 10.1016/j.psyneuen.2017.11.010 PMID: 29175720
- 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. doi: 10.1038/srep45203 PMID: 28327672
- 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. doi: 10.1186/s40779-022-00420-0 PMID: 36253804
- 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. doi: 10.1176/appi.ajp.2016.16040442 PMID: 28103712
- 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. doi: 10.4088/JCP.20m13469 PMID: 34004092
- 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. doi: 10.2174/1570159X19666210920090547 PMID: 34544343
- 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. doi: 10.2174/1570159X19666211111123918 PMID: 34766896
- 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. doi: 10.1016/j.schres.2016.09.026 PMID: 27743650
- 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. doi: 10.1016/j.eurpsy.2016.10.001 PMID: 28049080
- 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. doi: 10.1093/ijnp/pyaa097 PMID: 33315097
- 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. doi: 10.1001/jamapsychiatry.2016.3803 PMID: 28097367
- 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. doi: 10.1016/j.neuropharm.2019.05.010 PMID: 31077731
- 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. doi: 10.1055/s-2007-960492 PMID: 17479443
- 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. doi: 10.1007/s00125-018-4733-9 PMID: 30306190
- 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. doi: 10.1007/s00592-013-0493-7 PMID: 23836327
- 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. doi: 10.1089/thy.2016.0055 PMID: 27599541
- 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. doi: 10.1159/000475993 PMID: 28614818
- Pintana, H.; Chattipakorn, N.; Chattipakorn, S. Testosterone deficiency, insulin-resistant obesity and cognitive function. Metab. Brain Dis., 2015, 30(4), 853-876. doi: 10.1007/s11011-015-9655-3 PMID: 25703239
- 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. doi: 10.1186/1477-7827-11-106 PMID: 24238614
- 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. doi: 10.1155/2015/916585 PMID: 25883987
- Brzezinski-Sinai, N.A.; Brzezinski, A. Schizophrenia and sex hormones: What is the link? Front. Psychiatry, 2020, 11, 693. doi: 10.3389/fpsyt.2020.00693 PMID: 32760302
- 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. doi: 10.1111/bph.14584 PMID: 30658014
- 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 200105: An epidemiological survey. Lancet, 2009, 373(9680), 2041-2053. doi: 10.1016/S0140-6736(09)60660-7 PMID: 19524780
- 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. doi: 10.1038/sj.npp.1300157 PMID: 12700715
- 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. doi: 10.1038/s41380-019-0478-1 PMID: 31409883
- 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. doi: 10.1016/j.ijchp.2023.100402 PMID: 37663043
- 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. doi: 10.1038/s41537-023-00346-z PMID: 36949120
- Plum, L.; Schubert, M.; Brüning, J.C. The role of insulin receptor signaling in the brain. Trends Endocrinol. Metab., 2005, 16(2), 59-65. doi: 10.1016/j.tem.2005.01.008 PMID: 15734146
- 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. doi: 10.1001/jamapsychiatry.2019.0304 PMID: 30942838
- 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. doi: 10.1179/174313211X12966635733358 PMID: 21535919
- 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. doi: 10.1016/j.schres.2006.02.009 PMID: 16581231
- 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. doi: 10.1038/ng1296 PMID: 14745448
- 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. doi: 10.1016/j.eurpsy.2019.08.012 PMID: 31590015
- 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. doi: 10.1016/j.schres.2019.01.031 PMID: 30760413
- 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. doi: 10.1038/nature11007 PMID: 22622581
- 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 chickenegg dilemma. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2014, 48, 287-294. doi: 10.1016/j.pnpbp.2012.09.016 PMID: 23085507
- Peters, A. The selfish brain: Competition for energy resources. Am. J. Hum. Biol., 2011, 23(1), 29-34. doi: 10.1002/ajhb.21106 PMID: 21080380
- Veldhuis, J.D. Neuroendocrine mechanisms mediating awakening of the human gonadotropic axis in puberty. Pediatr. Nephrol., 1996, 10(3), 304-317. doi: 10.1007/BF00866767 PMID: 8792395
- 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. doi: 10.3390/ijms22010373 PMID: 33396472
- Gonçalves, V.F.; Cuperfain, A.B.; Kennedy, J.L. Sex differences in schizophrenia: estrogen and mitochondria. Neuropsychopharmacology, 2019, 44(1), 216-217. doi: 10.1038/s41386-018-0228-0 PMID: 30294000
- 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. doi: 10.1007/s00213-013-3415-z PMID: 24481565
- 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. doi: 10.1016/j.biopsych.2007.03.001 PMID: 17544382
- Kulkarni, J.; Gavrilidis, E.; Worsley, R.; Hayes, E. Role of estrogen treatment in the management of schizophrenia. CNS Drugs, 2012, 26(7), 549-557. doi: 10.2165/11630660-000000000-00000 PMID: 22626057
- Brandt, N.; Fester, L.; Rune, G.M. Neural sex steroids and hippocampal synaptic plasticity. Vitam. Horm., 2020, 114, 125-143. doi: 10.1016/bs.vh.2020.06.001 PMID: 32723541
- 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. doi: 10.1111/jne.13216
- 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. doi: 10.1016/j.yhbeh.2015.04.023 PMID: 25989597
- 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. doi: 10.1016/j.gendis.2021.01.007 PMID: 35873026
- 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. doi: 10.1016/j.jpsychires.2021.08.022 PMID: 34450525
- Mauvais-Jarvis, F. Role of sex steroids in β cell function, growth, and survival. Trends Endocrinol. Metab., 2016, 27(12), 844-855. doi: 10.1016/j.tem.2016.08.008 PMID: 27640750
- 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. doi: 10.1111/j.1743-6109.2009.01467.x PMID: 19732305
- 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. doi: 10.2164/jandrol.111.016089 PMID: 22441765
- 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. doi: 10.1530/JOE-11-0289 PMID: 22010203
- 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. doi: 10.1016/j.acthis.2009.10.004 PMID: 20149418
- Fanelli, G.; Gevi, F.; Belardo, A.; Zolla, L. Metabolic patterns in insulin-sensitive male hypogonadism. Cell Death Dis., 2018, 9(6), 653. doi: 10.1038/s41419-018-0588-8 PMID: 29844353
- 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. doi: 10.1111/and.13035 PMID: 29744905
- Melcangi, R.C.; Panzica, G.; Garcia-Segura, L.M. Neuroactive steroids: focus on human brain. Neuroscience, 2011, 191, 1-5. doi: 10.1016/j.neuroscience.2011.06.024 PMID: 21704130
- Reddy, D.S. Neurosteroids. Prog. Brain Res., 2010, 186, 113-137. doi: 10.1016/B978-0-444-53630-3.00008-7 PMID: 21094889
Supplementary files
