Zoueietal. BMC Res Notes (2018) 11:365
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
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Toxoplasma gondii is one of the most common parasitic
protozoans in humans which cause toxoplasmosis .
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 . erefore,
the accurate diagnosis of acute maternal toxoplasmosis
in pregnant women is critical . 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 .
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 . 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 . 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
BMC Research Notes
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.
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.
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. .
e OD of each sample was compared with cut oﬀ and
Antigen was prepared as previously described . 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
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.
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 . 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 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 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).
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 . 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 . Interestingly, castrated
male rats do not exhibit loss of fear phenotype, suggest-
ing that testosterone plays a direct role in this behavior
. 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 . 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 .
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 . 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 . 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 . 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 . 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
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
(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 .
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 . erefore, the parasite genotype
seems to be an important parameter inﬂuencing the clin-
ical infection in humans . 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 . 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 . 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.
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.
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.
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
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.
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
The study received no speciﬁc funding.
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional aﬃliations.
Received: 10 March 2018 Accepted: 1 June 2018
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