Associations between Toxoplasma gondii infection and steroid hormone levels in spotted hyenas

Abdelazeem, 2015, Assessment of level of cortisol hormone in patients with toxoplasmosis, Int. J. Sci. Res., 4, 55 Abdoli, 2014, Toxoplasma, testosterone, and behavior manipulation: the role of parasite strain, host variations, and intensity of infection, Front. Biol., 9, 151, 10.1007/s11515-014-1291-5 Abdoli, 2012, Impaired reproductive function of male rats infected with Toxoplasma gondii, Andrologia, 44, 679, 10.1111/j.1439-0272.2011.01249.x Abdulai-Saiku, 2017, Loss of predator aversion in female rats after Toxoplasma gondii infection is not dependent on ovarian steroids, Brain Behav. Immun., 65, 95, 10.1016/j.bbi.2017.04.005 Adkins-Regan, 2005 Agis-Balboa, 2009, Enhanced fear responses in mice treated with anabolic androgenic steroids, Neuroreport, 20, 617, 10.1097/WNR.0b013e32832a2393 Al-Masoudi, 2018, Molecular and hormonal study(Testosterone and luteinizing hormone) among applicants for marriage and blood donors peoples who infected with Toxoplasma gondii in Babylon Province, Iraq, J. Pharmaceut. Sci. Res., 10, 2391 Babu, 2007, Congenital toxoplasmosis presenting as hypogonadotropic hypogonadism, Indian J. Pediatr., 74, 577, 10.1007/s12098-007-0096-9 Berenreiterová, 2011, The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: implications for the behavioral manipulation hypothesis, PLoS One, 6, 10.1371/journal.pone.0028925 Bereshchenko, 2018, Glucocorticoids, sex hormones, and immunity, Front. Immunol., 9, 1, 10.3389/fimmu.2018.01332 Borráz-León, 2021, Toxoplasma gondii and psychopathology: latent infection is associated with interpersonal sensitivity, psychoticism, and higher testosterone levels in men, but not in women, Adapt. Hum. Behav. Physiol., 7, 28, 10.1007/s40750-020-00160-2 Colosi, 2015, Influence of Toxoplasma gondii infection on male fertility: a pilot study on immunocompetent human volunteers, Iran. J. Parasitol., 10, 402 Cooper, 1999, A seasonal feast: long-term analysis of feeding behaviour in the spotted hyaena (Crocuta crocuta), Afr. J. Ecol., 37, 149, 10.1046/j.1365-2028.1999.00161.x Di Cristina, 2008, Temporal and spatial distribution of Toxoplasma gondii differentiation into bradyzoites and tissue cyst formation in vivo, Infect. Immun., 76, 3491, 10.1128/IAI.00254-08 Dloniak, 2004, Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta), Gen. Comp. Endocrinol., 135, 51, 10.1016/j.ygcen.2003.08.011 Dubey, 1998, Advances in the life cycle of Toxoplasma gondii, Int. J. Parasitol., 28, 1019, 10.1016/S0020-7519(98)00023-X Dubey, 2016, Toxoplasmosis of animals and humans, second Elmore, 2010, Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention, Trends Parasitol., 26, 190, 10.1016/j.pt.2010.01.009 Eslamirad, 2013, Effects of Toxoplasma gondii infection in level of serum testosterone in males with chronic toxoplasmosis, Iran. J. Parasitol., 8, 622 Flegr, 2008, Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans, Parasitology, 135, 427, 10.1017/S0031182007004064 Fox, 2019 Frank, 1990, Sexual dimorphism in the spotted hyaena (Crocuta crocuta), J. Zool., 221, 308, 10.1111/j.1469-7998.1990.tb04001.x Gering, 2021, Toxoplasma gondii infections are associated with costly boldness toward felids in a wild host, Nat. Commun., 12, 10.1038/s41467-021-24092-x Glickman, 1992, Hormonal correlates of “masculinization” in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity, J. Reprod. Fertil., 95, 451, 10.1530/jrf.0.0950451 Graham, 2007, How many imputations are really needed? Some practical clarifications of multiple imputation theory, Prev. Sci., 8, 206, 10.1007/s11121-007-0070-9 Hamdeh, 2015, Intracranial toxoplasmosis presenting as panhypopituitarism in an immunocompromised patient, Am. J. Emerg. Med., 33, 1848.e1, 10.1016/j.ajem.2015.04.071 Hassanain, 2017, Comparative hormonal and immunoglobulin profiles of aborted women with or without toxoplasmsis, J. Pregnancy Reprod., 2, 1 Heany, 2015, A quantitative and qualitative review of the effects of testosterone on the function and structure of the human social-emotional brain, Metab. Brain Dis., 31, 157, 10.1007/s11011-015-9692-y Holekamp, 1996, Rank and reproduction in the female spotted hyaena, J. Reprod. Fertil., 108, 229, 10.1530/jrf.0.1080229 Holekamp, 2003, Effects of dispersal status on pituitary and gonadal function in the male spotted hyena, Horm. Behav., 44, 385, 10.1016/j.yhbeh.2003.06.003 Holekamp, 1998, Behavioral development in the spotted hyena, Bioscience, 48, 997, 10.2307/1313456 Holekamp, 1998, Dispersal status influences hormones and behavior in the male spotted hyena, Horm. Behav., 33, 205, 10.1006/hbeh.1998.1450 Holekamp, 1997, Hunting rates and hunting success in the spotted hyena (Crocuta crocuta), J. Zool., 242, 1, 10.1111/j.1469-7998.1997.tb02925.x Ihara, 2016, Toxoplasma gondii infection in mice impairs long-term fear memory consolidation through dysfunction of the cortex and amygdala, Infect. Immun., 84, 2861, 10.1128/IAI.00217-16 Kaňková, 2010, Modulation of immunity in mice with latent toxoplasmosis-the experimental support for the immunosuppression hypothesis of Toxoplasma-induced changes in reproduction of mice and humans, Parasitol. Res., 107, 1421, 10.1007/s00436-010-2013-9 Kaňková, 2011, Direct evidence of Toxoplasma-induced changes in serum testosterone in mice, Exp. Parasitol., 128, 181, 10.1016/j.exppara.2011.03.014 Korte, 2001, Corticosteroids in relation to fear, anxiety and psychopathology, Neurosci. Biobehav. Rev., 25, 117, 10.1016/S0149-7634(01)00002-1 Laubach, 2021, A biologist's guide to model selection and causal inference, Proc. R. Soc. B Biol. Sci., 10.1098/rspb.2020.2815 Lim, 2013, Toxoplasma gondii infection enhances testicular steroidogenesis in rats, Mol. Ecol., 22, 102, 10.1111/mec.12042 McConkey, 2013, Toxoplasma gondii infection and behaviour - location, location, location?, J. Exp. Biol., 216, 113, 10.1242/jeb.074153 McEwen, 2016, Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex, Neuropsychopharmacology, 41, 3, 10.1038/npp.2015.171 Mitra, 2013, Toxoplasma gondii infection induces dendritic retraction in basolateral amygdala accompanied by reduced corticosterone secretion, Dis. Model. Mech., 6, 516 Oktenli, 2004, Transient hypogonadotrophic hypogonadism in males with acute toxoplasmosis : suppressive effect of interleukin-1 b on the secretion of GnRH, Hum. Reprod., 19, 859, 10.1093/humrep/deh161 Shirbazou, 2011, Effects of Toxoplasma gondii infection on plasma testosterone and cortisol level and stress index on patients referred to Sina Hospital, Tehran, Jundishapur J. Microbiol., 4, 167 Singh, 2020, Testosterone acts within the medial amygdala of rats to reduce innate fear to predator odor akin to the effects of Toxoplasma gondii infection, Front. Psychiatr., 11, 7, 10.3389/fpsyt.2020.00630 Soravia, 2006, Glucocorticoids reduce phobic fear in humans, Proc. Natl. Acad. Sci. U.S.A., 103, 5585, 10.1073/pnas.0509184103 Stahl, 1994, Reproductive failure in mice chronically infected with Toxoplasma gondii, Parasitol. Res., 80, 22, 10.1007/BF00932619 Succop, 2004, Imputation of data values that are less than a detection limit, J. Occup. Environ. Hyg., 1, 436, 10.1080/15459620490462797 Tong, 2019, Testosterone reduces fear and causes drastic hypomethylation of arginine vasopressin promoter in medial extended amygdala of male mice, Front. Behav. Neurosci., 13, 1, 10.3389/fnbeh.2019.00033 van Buuren, 2011, mice: multivariate imputation by chained equations in R, J. Stat. Software, 45, 1 Van Meter, 2009, Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas, Horm. Behav., 55, 329, 10.1016/j.yhbeh.2008.11.001 Vyas, 2015, Extended epigenotype in a Rattus novergicus - Toxoplasma gondii association, Commun. Integr. Biol., 8, 9, 10.4161/19420889.2014.992743 Vyas, 2007, Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors, Proc. Natl. Acad. Sci. Unit. States Am., 104, 6442, 10.1073/pnas.0608310104 Vyas, 2010, Manipulation of host behaviour by Toxoplasma gondii: what is the minimum a proposed proximate mechanism should explain?, Folia Parasitol., 57, 88, 10.14411/fp.2010.011 Webster, 2010, Toxoplasma gondii-altered host behaviour: clues as to mechanism of action, Folia Parasitol., 57, 95, 10.14411/fp.2010.012 Wyle, 1977, Immunosuppression by sex steroid hormones, Clin. Exp. Immunol., 27, 407 Zghair, 2015, The effect of toxoplasmosis on the level of some sex hormones in males blood donors in Baghdad, J. Parasit. Dis., 39, 393, 10.1007/s12639-013-0382-6 Zouei, 2018, The association of latent toxoplasmosis and level of serum testosterone in humans, BMC Res. Notes, 11, 1, 10.1186/s13104-018-3468-5