Available via license: CC BY
Content may be subject to copyright.
Zoueietal. BMC Res Notes (2018) 11:365
https://doi.org/10.1186/s13104-018-3468-5
RESEARCH NOTE
The association oflatent toxoplasmosis
andlevel ofserum testosterone inhumans
Nima Zouei, Saeedeh Shojaee, Mehdi Mohebali and Hossein Keshavarz*
Objectives: Latent toxoplasmosis modifies various hormones and behaviors in infected hosts and possibly involves
in etiology of different neurologic and psychiatric disorders. The aim of the current study was to assess possible
associations between latent toxoplasmosis and testosterone concentration in Toxoplasma infected and free subjects.
Briefly, 18–49 year-old participated in the study. After collected blood samples, sera were analyzed for the detection
of anti-Toxoplasma IgG antibody. Totally, 76 positive sera were selected as study group (38 from men and 38 from
women) and a same number of negative sera as control group.
Results: Comparison of testosterone concentrations and control groups showed that testosterone concentration
in study group was higher than that in control group with statistically significant difference (P = 0.024 and P = 0.043
for men and women, respectively). Significant differences were found in testosterone concentrations and anti-Toxo-
plasma IgG antibody levels in study and control groups (P < 0.05). Toxoplasmosis can affect the mean concentration
of serum testosterone in human. Alteration of testosterone during latent toxoplasmosis can result in alterations in
behavioral, physiologic and immunological parameters in long time.
Keywords: Toxoplasma gondii, Testosterone, Electro chemiluminescence immunoassay, Latent toxoplasmosis
© The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license,
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/
publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Introduction
Toxoplasma gondii is one of the most common parasitic
protozoans in humans which cause toxoplasmosis [1].
e prevalence of toxoplasmosis varies from 20 to 80%
in different parts of the world. Humans become infected
through the oral route by the consumption of raw or
undercooked meat contaminated with tissue cysts and
other food products, water or vegetables contaminated
with oocysts. Congenital infection can occur via verti-
cal transmission of T. gondii tachyzoites from pregnant
mother to developing fetus during the primary infection
that could be life threatening for the fetus [2]. erefore,
the accurate diagnosis of acute maternal toxoplasmosis
in pregnant women is critical [3]. Latent toxoplasmosis
is clinically asymptomatic in immunocompetent hosts.
However, the infection is usually long-lasting character-
ized by the presence of Toxoplasma cysts, typically in
nervous and muscular tissues. Furthermore, the infection
mostly results in a lifetime protective immunity (humoral
and cellular) to reinfection, presenting low levels of anti-
Toxoplasma IgG in serum of infected individuals [4].
Latent toxoplasmosis is known to induce various hor-
monal and behavioral changes in infected humans and
animals and may be involved in etiology of different neu-
rologic and psychiatric disorders [5–7]. Infected mice
and rats have been shown to suffer from impaired motor
neuron performance and coordination, deficit learning
and reduced avoidance of open spaces and predators
[8–12]. ese are believed to be evolutionary mecha-
nisms to increase the chance of hosts being eaten by
felines [13]. Furthermore, latent toxoplasmosis increases
chance of giving birth to males in humans and mice [14,
15]. Patients with changed testosterone levels may expe-
rience physical symptoms such as dermal hyper reactions
including irritation, erythema, hirsutism and acne as well
as abnormal growth of muscles, kidney failure and psy-
chological deficits such as mood swings, depression and
anxiety [16]. An effect of latent toxoplasmosis on serum
testosterone changes is still being discussed by research-
ers. Published data have shown increased and decreased
testosterone levels associated with T. gondii seropositivity
Open Access
BMC Research Notes
*Correspondence: hkeshavarz@tums.ac.ir
Department of Medical Parasitology and Mycology, Tehran
University of Medical Sciences, Pour Sina St., Ghods St., Enghelab St.,
Tehran 1417613191, Iran
Page 2 of 5
Zoueietal. BMC Res Notes (2018) 11:365
in humans [17–19]. In the current study, effects of latent
toxoplasmosis on serum testosterone were assessed in
men and women.
Main text
Methods
Samples andpatients
In this case–control study, 18–49 year-old men and
women with no clinical complications were participated.
Blood samples were collected in clinical laboratories in
Tehran, May–September 2013. Information sheets were
prepared and demographic questionnaires completed
for the participants. en, 3 ml of whole blood were
collected and sera were tested for the detection of anti-
Toxoplasma IgG antibody. In total, 76 positive sera were
selected as study group (equally from men and women)
and further 76 negative as control group.
Serological tests
Enzyme-linked immunosorbent assay (ELISA) was used
to detection of anti-Toxoplasma IgG antibody in blood
sera. e cut off values of optical densities (OD) were
calculated according to a protocol by Hillyer etal. [20].
e OD of each sample was compared with cut off and
recorded.
Antigen preparation
Antigen was prepared as previously described [21]. e
RH strain of T. gondii was obtained from the Depart-
ment of Parasitology, Tehran University of Medical Sci-
ences, Tehran, Iran. Briefly, tachyzoites of T. gondii, RH
strain were inoculated intraperitoneally into BALB/c
mice. After 48–72 h, tachyzoites were collected using
peritoneum washing with sterile normal saline (pH 7.2).
Tachyzoites were washed with phosphate-buffered saline
(PBS pH 7.4) for three times, sonicated in PBS (pH 7.4)
and centrifuged at 12,000g for 1h at 4°C. en, super-
natants were collected and protein density was assessed
using Bradford method. Animal experiments were done
according to Committee for the Update of the Guide for
the Care and Use of Laboratory Animals and approved by
the Ethical Committee of Tehran University of Medical
Sciences for the use of laboratory animals.
Detection ofanti‑Toxoplasma IgG antibody using ELISA
technique
e 96-well microplates (Nunk, Germany) were coated
with 5 µg/ml of soluble antigen of T. gondii RH strain
in carbonate-bicarbonate buffer (pH 9.6) and stored at
4°C. Plates were washed for three times with PBST (PBS,
0.05% tween 20) and sera were diluted 1:200 in PBST and
100µl from diluted sera was added to each well of micro-
plate. After incubation for 1h at 37°C and three times
of washing, 100 µl of anti-human IgG conjugated with
hourseradish peroxidase (HRP) (Dako, Denmark) diluted
1:500 in PBST and added to each well. After incubating
and washing, 100 µl of substrate of ortho-phenylenedi-
amine (OPD) (Sigma-Aldrich, USA) was added to wells.
e catalytic enzyme was stopped by adding 50 µl of
20% sulfuric acid at a specific time and the absorbance
was measured at 490nm using automated ELISA reader
(BIOTEC LX800, USA). Furthermore, all samples were
approved for the determination of anti-Toxoplasma IgG
using commercial kits (Trinity Biotech Captia, New York,
USA) according to the manufacturer’s instructions.
Testosterone assessment
Concentration of testosterone was assessed at 37°C using
Roche Cobas® e 411 Immunoassay (Roche Diagnostics,
Mannheim, Germany) according to the manufacturer’s
instructions. In the first incubation step, 20 μl of the
sample were incubated with a biotinylated monoclonal
testosterone-specific antibody and 2-bromoestradiol (to
release testosterone). In the second step, streptavidin-
coated microparticles and a ruthenylated testosterone
derivative were added to the mixture. e reaction mix-
ture was transferred to a measuring cell and the micro-
particles were magnetically captured on the surface of an
electrode. Chemiluminescence was measured using pho-
tomultiplier and the concentration of testosterone was
calculated using calibration curve [22]. Interpretation of
the testosterone concentration was based on the manu-
facturer’s recommendation as follows: normal range for
men, 2.49–8.36ng/ml; and for women, 0.084–0.481ng/
ml. Experiments were carried out in triplicate, and the
mean was calculated for each sample.
Statistical analysis
Statistical analyses were carried out using SPSS Software
v.16. Data were analyzed using multiple univariate analy-
ses of variance (ANOVA) and Chi square test. Pearson
product-moment correlations were used between opti-
cal density of ELISA and concentration of testosterone.
Comparison of quantitative variants between two groups
was assessed by student t test. Data description was car-
ried out by calculating frequencies and 95% confidence
intervals. Differences were considered as significant
when P ≤ 0.05.
Results
Results of anti-Toxoplasma IgG antibody detection
and serum testosterone concentration in infected and
non-infected subjects are shown in Table1. Differences
in mean concentrations of testosterone were reported
between infected and non-infected subjects (P < 0.05)
as testosterone concentration was significantly higher
Page 3 of 5
Zoueietal. BMC Res Notes (2018) 11:365
in IgG-positive group than that in IgG-negative one. In
infected subjects, 13.2 and 26.3% of men and women
had high concentrations of serum testosterone, respec-
tively. e mean concentration of serum testosterone was
higher in men and women infected by T. gondii and sta-
tistically significant (P = 0.02 and P = 0.04, resp ectively),
compared to that in control group. Furthermore, corre-
lation between the mean OD of ELISA and concentra-
tion of testosterone was significant in infected men and
women with values of 0.007 and 0.004, respectively. No
statistically significant association was found between
IgG titers and testosterone levels in men and women in
Toxoplasma seropositivity group in comparison with
control group (P > 0.05).
Discussion
Parasite-induced changes to the host endocrine system
provide a possible mechanism of altering host behav-
iors. Significant sex differences have been reported
regarding host changes in response to T. gondii infec-
tion [19]. Testosterone is an important influencing fac-
tor in behavior and personality in both sexes. As shown
in majority of the studies, increased testosterone was
associated with antisocial, aggression and dominance
behaviors [23–25]. Altered testosterone levels have been
observed in T. gondii infections; however the literatures
lack consensuses. Evidence suggests that testosterone
activation may cause sexual arousal directed towards
feline odor in some rodents [26]. Interestingly, castrated
male rats do not exhibit loss of fear phenotype, suggest-
ing that testosterone plays a direct role in this behavior
[27]. Results of the current study have shown that mean
concentrations of serum testosterone are significantly
higher in men and women infected by toxoplasmosis,
compared to that in control group. Increased concen-
tration of testosterone during latent toxoplasmosis can
result in inducted behavioral alterations and immuno-
suppressive effects characterized by lower cellular immu-
nity [25, 28]. Administration of exogenous testosterone
can reduce fear in humans and rodents [29]. It is possi-
ble that men with increased levels of testosterone have
greater chance of Toxoplasma infection either due to
impaired immunity or changed behavior and personality
profile. For instance, personal tendency to disregard rules
of the society can result in lower hygienic standards and
hence increase risk of contact with sources of infection
[30–33]. e underlying mechanism for these behavioral
alterations are usually thought to be variations in neuro-
transmitter functions and more specifically due to high
levels of dopamine. In addition, there are indications that
enhanced testosterone levels play an important role in
behavioral abnormalities [34].
Several studies have shown that, direct and indirect
evidence exist on increased testosterone in Toxoplasma
infected human and animals [35–39]. T. gondii produces
high concentrations of testosterone in infected hosts
and enhanced mRNA expression of luteinizing hormone
receptor (LHR), which regulate the synthesis of testos-
terone in testes on Leydig cells [27]. e Toxoplasma
infected men are about 3cm taller than Toxoplasma free
men and having further muscles and dominant faces [38,
39]. Toxoplasma infected men and women have a lower
second to fourth digit length ratio in the left hand (2D:4D
ratio) and are more likely to give birth to boys than
girls [14, 40]. e findings of current study is in accord-
ance with James hypothesis (2010) that many parasites
and pathogens could change the concentration of ster-
oid hormone. He has demonstrated that infected hosts,
often with shifted sex ratio, increase number of males
in generations [40]. Testosterone is a hormone which
is responsible for the growth of secondary male sexual
characteristics. An alternative hypothesis explaining Tox-
oplasma associated sex ratio shift suggests that the phe-
nomenon is caused by the higher possibility of survival of
more immunogenic male embryos by inducing immuno-
suppression mechanisms [30]. Indeed, both hypotheses
may be compatible since the proximate mechanism of
immunosuppression remains unknown and may involve
the parasite-induced shift in steroid hormones.
e results of present study do not agree with Flegr
etal. showed that Toxoplasma infected men had a higher
concentration of testosterone while women had a lower
concentration of the hormone, compared to control
group [19]. Furthermore, Flegr suggested that the per-
sonality profiles of infected men and women are differ-
ent and the opposite direction of the testosterone shift in
men compared to women can explain the observed gen-
der specificity of behavioral changes in people infected
with Toxoplasma parasite. ey have concluded that
infected women are warm-hearted, conscientious, out-
going, persistent, and moralistic while infected men are
Table 1 Mean OD of ELISA and concentration
of testosterone (ng/ml) in 18–49 year-old infected men
andwomen, compared tothatin non-infected ones
Group Mean OD ± SD Mean concentration
oftestosterone (ng/
ml) ± SD
Infected men 1.05 ± 0.53 5.6 ± 1.99
Infected women 0.94 ± 0.37 0.41 ± 0.22
Non-infected men (sero-
negative) 0.14 ± 0.08 4.56 ± 1.96
Non-infected women
(sero-negative) 0.15 ± 0.08 0.31 ± 0.17
Page 4 of 5
Zoueietal. BMC Res Notes (2018) 11:365
more likely to disregard rules and were more expedient,
suspicious, jealous, and dogmatic [19].
Contrary to our results, a controversial study by Kank-
ova etal. has shown a decrease testosterone levels (total
testosterone and free testosterone) in female and male
laboratory mice infected by virulent strains of Toxo-
plasma at a latent phase, compared to uninfected con-
trols. is controversy may be seen due to the different
parasite strain, which differs in virulence and epidemio-
logical occurrence [41]. erefore, the parasite genotype
seems to be an important parameter influencing the clin-
ical infection in humans [42]. It is possible that the physi-
ological reaction to Toxoplasma infection qualitatively
differs between mice and humans. Other reports show
that reduced serum and testicular testosterone levels was
found in male rats infected by high doses of T. gondii, RH
strain compared to controls [43]. Similarly, Oktenli etal.
have demonstrated that concentration of follicle stimu-
lating hormone (FSH), luteinizing hormone (LH), free
testosterone (FT) and total testosterone(TT) were sig-
nificantly lower than controls in serum of male patients
during acute toxoplasmosis [44]. Results of the current
study showed that the mean concentration of serum
testosterone was higher in men and women infected by
toxoplasmosis, compared to that in control group. Of
various mechanisms described in T. gondii for behavioral
alterations, increased testosterone seems to play a signifi-
cant role. Alterations of testosterone during latent toxo-
plasmosis can affect several behavioral, physiologic and
immunological parameters in a long time.
Limitations
In this study the association of latent toxoplasmosis and
psychological disorders was not tested in patients. It is
suggested to further investigation of direct correlation
between latent toxoplasmosis and psychological disor-
ders in animal and human models.
Abbreviations
ECLIA: electro chemiluminescence immunoassay; ELISA: enzyme-linked
immunosorbent assay; IgG: immunoglobulin G; PBST: phosphate buffered
saline, tween 20; HRP: hourseradish peroxidase; OPD: ortho phenylenedi-
amine; OD: optical density; 2D:4D ratio: second to fourth digit length ratio;
SPSS: statistical package for the social sciences; FSH: follicle stimulating
hormone; LH: luteinizing hormone.
Author contributions
HK designed the experiments and provided important advice for the experi-
ments and financial support. NZ collected the samples and performed the
experiments. MM and SS analyzed and interpreted the data and contributed
to manuscript preparation. NZ drafted the original manuscript. HK, SS and MM
reviewed and revised the manuscript. All authors read and approved the final
manuscript.
Acknowledgements
The authors would like to thank staff within the toxoplasmosis laboratory,
Department of Medical Parasitology and Mycology, Tehran University of Medi-
cal Sciences, Tehran, Iran, for their useful collaboration.
Competing interests
The authors declare no competing interests.
Availability of data and materials
Data that support the findings of this study are available on reasonable
request to the corresponding author.
Consent for publication
Not applicable (no individual person’s data).
Ethics approval and consent to participate
The study was approved by Ethical Committee of Tehran University of Medical
Sciences. Informed written consent was obtained from all participants before
being involved in the study. All participants signed an informed consent and
received a complete copy of the signed consent form
Funding
The study received no specific funding.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional affiliations.
Received: 10 March 2018 Accepted: 1 June 2018
References
1. Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton:
CRC Press Inc.; 2010. p. 1–313.
2. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to
humans. Int J Parasitol. 2000;30:1217–58.
3. Selseleh M, Keshavarz H, Mohebali M, Shojaee S, Selseleh M, Eshragian
MR, Mansouri F, Modarressi MH. Production and evaluation of Toxoplasma
gondii recombinant GRA7 for serodiagnosis of human infections. Korean J
Parasitol. 2012;50:233–8.
4. Weiss LM, Dubey JP. Toxoplasmosis: a history of clinical observations. Int J
Parasitol. 2009;39(8):895–901.
5. Webster JP. Rats, cats, people and parasites: the impact of latent toxoplas-
mosis on behaviour. Microbes Infect. 2001;3:1037–45.
6. Mahmoudvand H, Ziaalia N, Ghazvini H, et al. Toxoplasma gondii infection
promotes neuroinflammation through cytokine networks and induced
hyperalgesia in BALB/c mice. Inflammation. 2016;39:405–12.
7. Alipour A, Shojaee S, Mohebali M, Tehranidoost M, Abdi Masoleh F, Kes-
havarz H. Toxoplasma infection in schizophrenia patients: a comparative
study with control group. Iran J Parasitol. 2011;6(2):31–7.
8. Mahmoudvand H, Ziaali N, Aghaei I, Sheibani V, Shojaee S, Keshavarz H,
Shabani M. The possible association between Toxoplasma gondii infection
and risk of anxiety and cognitive disorders in BALB/c mice. Pathogen
Glob Health. 2016;109(8):369–76.
9. Mahmoudvand H, Sheibani V, Shojaee S, Mirbadie SR, Keshavarz H,
Esmaeelpour K, Keyhani AR, Ziaali N. Toxoplasma gondii infection potenti-
ates cognitive impairments of Alzheimer’s disease in the BALB/C mice. J
Parasitol. 2016;102(6):629–35.
10. Hutchinson WM, Bradley M, Cheyne WM, Wells BW, Hay J. Behavioural
abnormalities in Toxoplasma-infected mice. Ann Trop Med Parasitol.
1980;74:337–45.
11. Witting PA. Learning capacity and memory of normal and Toxoplasma-
infected laboratory rats and mice. Z fur Parasitenkd. 1979;61:29–51.
Page 5 of 5
Zoueietal. BMC Res Notes (2018) 11:365
•
fast, convenient online submission
•
thorough peer review by experienced researchers in your field
•
rapid publication on acceptance
•
support for research data, including large and complex data types
•
gold Open Access which fosters wider collaboration and increased citations
maximum visibility for your research: over 100M website views per year
•
At BMC, research is always in progress.
Learn more biomedcentral.com/submissions
Ready to submit your research
? Choose BMC and benefit from:
12. Skallova A, Kodym P, Frynta D, Flegr J. The role of dopamine in Toxo-
plasma-induced behavioural alterations in mice: an ethological and
ethopharmacological study. Parasitology. 2006;133:525–35.
13. Moore J. Parasites and the behavior of animals. Oxford: Oxford University
Press; 2002. ISBN 9780195146530.
14. Kankova S, Sulc J, Nouzova K, Fajfrlik K, Frynta D, Flegr J. Women infected
with parasite Toxoplasma have more sons. Naturwissenschaften.
2007;94:122–7.
15. Kankova S, Kodym P, Frynta D, Vavrinova R, Kubena A, Flegr J. Influence
of latent toxoplasmosis on the secondary sex ratio in mice. Parasitology.
2007;134:1709–17.
16. Cox RM, John-Alder HB. Testosterone has opposite effects on male
growth in lizards (Sceloporus spp.) with opposite patterns of sexual size
dimorphism. J Exp Biol. 2005;208:4679–87.
17. Zghair KH, AL-Qadhi BN, Mahmood SH. The effect of toxoplasmosis on
the level of some sex hormones in males blood donors in Baghdad. J
Parasit Dis. 2015;39:393–400.
18. Eslamirad Z, Hajihossein R, Ghorbanzadeh B, Alimohammadi M, Mosayebi
M, Didehdar M. Effects of Toxoplasma gondii infection in level of serum
testosterone in males with chronic toxoplasmosis. Iran J Parasitol.
2013;8:622–6.
19. Flegr J, LIindova J, Kodym P. Sex-dependent toxoplasmosis-associated
differences in testosterone concentration in humans. Parasitology.
2008;135:427–31.
20. Hillyer GV, de Galanes MS, Rodriguez-Perez J, Bjorland J, de Lagrava MS,
Guzman SR, et al. Use of the falcon assay screening test–enzyme-linked
immunosorbent assay (FAST-ELISA) and the enzyme-linked immunoelec-
trotransfer blot (EITB) to determine the prevalence of human fascioliasis
in the Bolivian Altiplano. Am J Trop Med Hyg. 1992;46(5):603–9.
21. Teimouri A, Azami SJ, Keshavarz H, Esmaeili F, Alimi R, Mavi SA, Shojaee
S. Anti-Toxoplasma activity of various molecular weights and concen-
trations of chitosan nanoparticles on tachyzoites of RH strain. Int J
Nanomed. 2018;13:1341–51.
22. Teimouri A, Modarressi MH, Shojaee S, et al. Detection of toxoplasma-
specific immunoglobulin G in human sera: performance comparison of
in house Dot-ELISA with ECLIA and ELISA. Eur J Clin Microbiol Infect Dis.
2018. https ://doi.org/10.1007/s1009 6-018-3266-y.
23. Booth A, Granger DA, Mazur A, Kivlighan KT. Testosterone and social
behavior. Soc Forces. 2006;85(1):167–91.
24. Eisenegger C, Haushofer J, Fehr E. The role of testosterone in social inter-
action. Trends Cogn Sci. 2011;15(6):263–71.
25. Montoya ER, Terburg D, Bos PA, van Honk J. Testosterone, cortisol, and
serotonin as key regulators of social aggression: a review and theoretical
perspective. Motiv Emot. 2012;36(1):65–73.
26. House PK, Vyas A, Sapolsky R. Predator cat odors activate sexual arousal
pathways in brains of Toxoplasma gondii infected rats. PLoS ONE.
2011;6:e23277.
27. Lim A, Kumar V, Dass SAH, Vyas A. Toxoplasma gondii infection enhances
testicular steroidogenesis in rats. Mol Ecol. 2013;22:102–10.
28. Roberts F, Mets M, Ferguson N, Grady R. Histopathological features of
ocular toxoplasmosis in fetus and infant. J Opthal. 2001;119(1):51–8.
29. Abdoli A. Toxoplasma, testosterone, and behavior manipulation: the role
of parasite strain, host variations, and intensity of infection. Front Biol.
2014;9(2):151–60.
30. Kankova S, Holan V, Zajicova A, Kodym P, Flegr J. 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. 2010;107:1421–7.
31. Lindova J, Novotna M, Havlicek J, Jozifkova E, Skallova A, Kolbekova P,
Hodny Z, Kodym P, Flegr J. Gender differences in behavioural changes
induced by latent toxoplasmosis. Int J Parasitol. 2006;36:1485–92.
32. Lindova J, Kubena AA, Sturcova H, Krivohlava R, Novotna M, Rubesova
A, Havlicek J, Kodym P, Flegr J. Pattern of money allocation in experi-
mental games supports the stress hypothesis of gender differences
in Toxoplasma gondii-induced behavioural changes. Folia Parasitol.
2010;57:136–42.
33. Flegr J. Influence of latent toxoplasmosis on the phenotype of intermedi-
ate hosts. Folia Parasitol. 2010;57:81–7.
34. Webster JP. Rats, cats, people and parasites: the impact of latent toxoplas-
mosis on behaviour. Microbes Infect. 2001. https ://doi.org/10.1016/S1286
-4579(01)01459 -9.
35. Hodkova H, Kolbekova P, Skallova A, Lindova J, Flegr J. Higher perceived
dominance in Toxoplasma infected men—a new evidence for role of
increased level of testosterone in toxoplasmosis- associated changes in
human behavior. Neuro Endocrinol Lett. 2007;28(2):110–4.
36. Shirbazou S, Abasian L, Meymand FT. Effects of Toxoplasma gondii
infection on plasma testosterone and cortisol level and stress index
on patients referred to Sina hospital, Tehran. Jundishapur J Microbiol.
2011;4:167–73.
37. Flegr J, Hruskov YM, Hodna Z, Novotna M, Hanusova J. Body height,
body mass index, waist-hip ratio, fluctuating asymmetry and second
to fourth digit ratio in subjects with latent toxoplasmosis. Parasitology.
2005;130(6):621–8.
38. Flegr J, Lindova J, Pivonkova V, Havlicek JB. Brief communication: latent
toxoplasmosis and salivary testosterone concentration important
confounding factors in second to fourth digit ratio studies. Am J Phys
Anthropol. 2008;137:479–84.
39. Flegr J. Influence of latent Toxoplasma infection on human personal-
ity, physiology and morphology: pros and cons of the Toxoplasma-
human model in studying the manipulation hypothesis. J Exp Biol.
2013;216(1):127–33.
40. Kratochvil L, Flegr J. Differences in the 2nd to 4th digit length ratio
in humans reflect shifts along the common allometric line. Biol Lett.
2009;5:643–6.
41. Kankova S, Kodym P, Flegr J. Direct evidence of Toxoplasma-induced
changes in serum testosterone in mice. Exp Parasitol. 2011;128:181–3.
42. Vallochi AL, Muccioli M, Martins C, Silveira C, Belfort R. The genotype of
Toxoplasma gondii strains causing ocular toxoplasmosis in humans in
Brazil. Am J Ophthalmol. 2005;139:350–1.
43. Abdoli A, Dalimi A, Movahedin M. Impaired reproductive function of
male rats infected with Toxoplasma gondii. Andrologia. 2012;44(Suppl
1):679–87.
44. Oktenli C, Doganci L, Ozgurtas T, Araz RE, Tanyuksel M, Musabak U,
Sanisoglu SY, Yesilova Z, Erbil MK, Inal A. Transient hypogonadotrophic
hypogonadism in males with acute toxoplasmosis: suppressive
effect of interleukin-1beta on the secretion of GnRH. Hum Reprod.
2004;19(4):859–66.
