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The association of latent toxoplasmosis and level of serum testosterone in humans

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Abstract

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-Toxoplasma 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.
Zoueietal. BMC Res Notes (2018) 11:365
https://doi.org/10.1186/s13104-018-3468-5
RESEARCH NOTE
The association oflatent toxoplasmosis
andlevel ofserum testosterone inhumans
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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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 [57]. 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
[812]. 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
Zoueietal. BMC Res Notes (2018) 11:365
in humans [1719]. In the current study, effects of latent
toxoplasmosis on serum testosterone were assessed in
men and women.
Main text
Methods
Samples andpatients
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 etal. [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 12,000g for 1h 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 ofanti‑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
100µl from diluted sera was added to each well of micro-
plate. After incubation for 1h 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 490nm 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, 2.49–8.36ng/ml; and for women, 0.084–0.481ng/
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 Table1. 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
Zoueietal. 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 [2325]. 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
[3033]. 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 [3539]. 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 3cm 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
etal. 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
andwomen, compared tothatin non-infected ones
Group Mean OD ± SD Mean concentration
oftestosterone (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
Zoueietal. 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 etal. 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 etal.
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
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... The personal information collected included age, marital status, residency (urban and rural), educational level (up to high school, undergraduate or higher), years of working experience as a butcher, and smoking status, including cigarettes, waterpipe, and electrical cigarettes. Three smoking levels were studied: mild (1-10), moderate (11)(12)(13)(14)(15)(16)(17)(18)(19)(20), and heavy smoking (more than 20), whereas waterpipe smoking was considered mild if less than once a week, moderate if one to six heads a week, and heavy if daily. ...
Article
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A cross-sectional study was conducted in 2024 to study the seroprevalence of Toxoplasma gondii (T. gondii) and male testosterone levels in Palestinian butchers in the West Bank. Sera were collected from 156 butchers and tested for anti-T. gondii-IgG and IgM using commercial immune assay and testosterone tests. Univariate and bivariate analyses were used to calculate crude and adjusted odds ratios. The seroprevalences were 62.8% for anti-T-gondii-IgG, 7.1% for anti-T-gondii-IgM, and 7.1% for both IgG and IgM. T. gondii-IgG seropositive individuals had a median testosterone level of 351 ng/dL, significantly lower than the 428.5 ng/dL observed in T. gondii-IgG seronegative participants (p = 0.017). T. gondii-IgG seropositivity was associated with raw meat consumption, exposure to soil, age, and years of practice with adjusted odd ratios of 3.85, 3.32, 1.10, and 1.27, respectively. However, low testosterone level was not significantly associated with T. gondii seropositivity (p = 0.07). This finding suggests that additional research is needed to understand the relationship between Toxoplasma infection and testosterone levels.
... Other studies have shown contrary results regarding hormonal dynamics, even when the disease is not in the acute phase. In 2018, Zouei et al. [33] studied the serum of 38 men who were IgG-positive for T. gondii by comparing their testosterone concentration with those of 38 men in a control group. The results were statistically significant (p = 0.02), with a greater average concentration of testosterone in infected men (5.6 ± 1.99 ng/mL) than in noninfected men (4.56 ± 1.96 ng/mL). ...
Article
Purpose Toxoplasmosis is a worldwide widespread parasitic infection; it affects about 30% of the global population, either through acute toxoplasmosis or its sequels. Even though the male reproductive system is not the primary target for Toxoplasma gondii (T. gondii), studies have inquired into the possibility of presenting repercussions in this system directly or indirectly due to toxoplasmosis. Therefore, this systematic literature review aims to summarize the available evidence on the effects of infection caused by T. gondii on the male reproductive tract. Methods We searched PubMed, Scopus, LILACS and Google Scholar until June 2024 to identify studies of T. gondii and the human male reproductive system. Finally, we analyzed 24 papers published between 1986 and 2024. The Joanna Briggs Institute (JBI) Critical Appraisal Checklist was used to assess the potential risk of bias and the quality of the results. Results Infertility is a multicausal issue, including various stages in which the infection caused by T. gondii could interfere, but the mechanisms are not fully understood yet. Studies in animals, particularly rats, have shown the harmful effects of the parasite on sperm performance and endocrine function. In the same way, sexual transmission of T. gondii has been extensively studied in animals, with the parasite detected in the semen of various species. In humans, this transmission route remains theoretical due to study limitations. However, discrepancies in findings call for further research to understand the mechanisms and make the T. gondii’s infection impact on the male reproductive system a topic of growing interest. Conclusion Acute and chronic infection by T. gondii in the male reproductive system is a topic of growing interest due to its possible implications for reproductive health.
... Kita hipotezė teigia, kad endokrininės sistemos pokyčiai, ypač padidėjusi testosterono raiška, gali lemti T. gondii užkrėstų šeimininkų elgesio pokyčius. Testosteronas yra svarbus veiksnys, turintis įtakos abiejų lyčių elgesiui ir asmenybei − padidėjęs testosterono kiekis yra susijęs su asocialiu, agresyviu ir dominuojančiu elgesiu [8]. Šią hipotezę pagrindžia in vivo tyrimai, kurie parodė, kad užsikrėtusių graužikų patinų testosterono koncentracija yra didesnė ir susilpnėja įgimtas savisaugos instinktas kačių šlapimo kvapui − jį pajutę graužikai netenka baimės jausmo, jaučia jam potraukį, todėl padidėja tikimybė, kad žiurkė taps katės grobiu. ...
Article
Toksoplazmozę sukeliantis parazitas Toxoplasma gondii (T. gondii) yra plačiai paplitęs tarpląstelinis pirmuonis, kurio pagrindinis infekcijos šaltinis žmonėms yra ka­tės. Nors dauguma lėtinės toksoplazmozės atvejų yra besimptomiai, ūminė T. gondii infekcija yra pavojinga pažeidžiamoms gyventojų grupėms ir gali pasireikšti į psichozę panašiais simptomais. Pastaruoju metu atsi­randa įrodymų, kad ir lėtinė toksoplazmozė gali būti susijusi su psichikos sutrikimais, tokiais kaip šizofrenija ir bipolinis afektinis sutrikimas (BAS), nors tikslus vei­kimo mechanizmas vis dar neaiškus. Tyrimo tikslas − išsamiai apžvelgti dabartinius literatūros duomenis apie toksoplazmozės ir šizofrenijos bei BAS ryšį. Tyrimo re­zultatai. Tyrimai parodė, kad parazito gebėjimas įsitvir­tinti smegenyse ir sutrikdyti neuromediatorių funkciją, sukelti neurouždegimą gali prisidėti prie šizofrenijos ir BAS atsiradimo. Nustatyta, kad toksoplazmozės anti­kūnų, rodančių lėtinę infekciją, paplitimas tarp šizofre­nija ir BAS sergančių pacientų yra didesnis lyginant su žmonėmis, nesergančiais šiomis psichiatrinėmis ligomis. Rasta įrodymų, kad yra ryšys tarp motinos užsikrėtimo toksoplazmozės infekcija ir padidėjusios šizofrenijos rizikos palikuonims, ypač kai antikūnai perduodami per placentą. Šizofrenija sergantiems asmenims tokso­plazmozės infekcija siejama su pakitusiu dopamino ir glutamato kiekiu bei padidėjusia neurotoksinių veiksnių įtaka. Panašiai ir BAS sergantiems pacientams tokso­plazmozės infekcija siejama su neurouždegimu ir ko­gnityviniais sutrikimais, ypač ligos paūmėjimų metu. Rezultatai parodė, kad tyrimų duomenys išlieka prieš­taringi – kai kurių tyrimų duomenimis, lėtinės tokso­plazmozės infekcijos ir psichikos sutrikimų sąsajos yra reikšmingos, tačiau kituose tyrimuose tokių sąsajų ne­rasta. Tokie veiksniai, kaip pacientų amžius ir gyvena­moji vieta, gali turėti įtakos šių tyrimų duomenims, o tai rodo, kad norint visapusiškai suprasti šią sudėtingą sąveiką, reikia tolesnių išsamių tyrimų.
... Lim et al. [20] referred to that the infection with T. gondii leading to a long-term increase of testosterone, where experimentally a Toxoplasma gondii attack the testes in laboratory rat [21][22] and making changes in the synthesis of testosterone and nucleus accumbal dopamine content in this animal model [20][21][22][23]. Zouei et al. [24] reported elevated of testosterone concentration in study group as compared to control group. ...
Chapter
Full-text available
Toxoplasma gondii is an obligate intracellular infects both humans and animals. T. gondii parasitize in different organs even in testes and it was isolated from semen. The level of testosterone in the serum was evaluated for men with chronic toxoplasmosis. One hundred twenty-one blood samples were collected from apparently healthy men with different age groups they were attending the teaching hospital in Al-Diwaniyah province. Three milliliters of blood drawn from each man, and then sera were separated by centrifugation. Anti-Toxoplasma IgG antibody was detected. Same numbers of positive and negative sera were included in cases and control groups respectively, and then the quantitative determination of testosterone was analyzed in the serum of both groups. Thirty eight (31.4%) out of 121 examined serum samples were given positive results for T. gondii IgG antibodies. The results indicated a high rate of infection among males in different age groups, especially in the 30-44 years group. The testosterone levels appeared that the hormone concentration was relatively higher in the case group than in the control group at ages 15-29 years with significant differences (P<0.05). People who live in cities compared to rural residents and those who keep cats compared to others recorded a higher rate (39. 14% and 35.71 % respectively) of anti-T. gondii IgG. We conclude from the current study that the rate of infection with T. gondii is high among men and increases during the active period of maturity and is affected by some risk factors such as type of housing and ownership of cats and has an impact on their testosterone levels.
... Por otra parte, Zouei et al., en su estudio demuestra que la población infectada por T. gondii tienen alteraciones a nivel hormonal, sin distinción del sexo, con un aumento significativo de los niveles de testosterona (p = 0,02 y p = 0,04 para hombres y mujeres, respectivamente) a diferencia del grupo control que no lo presenta. El aumento de testosterona se ha asociado a cambios conductuales, tales como, comportamientos antisociales, agresividad y conductas dominantes al igual que reacciones inmunosupresoras 43 . ...
Article
Full-text available
El Toxoplasma gondii es un parásito que se encuentra, aproximadamente, en el 30 % de la población humana. Durante los últimos años se ha evidenciado que la infección latente puede ser un factor de riesgo para el desarrollo de trastornos mentales; particularmente para la esquizofrenia, ansiedad, trastornos bipolares y trastornos de conducta. La asociación con los trastornos neuropsiquiátricos pueden explicarse por la influencia que tiene el parásito sobre la expresión de múltiples neurotransmisores; entre ellos la dopamina. Se realizó una búsqueda en las bases de datos PubMed y SciELO de 2015 a 2023, se seleccionaron artículos originales y de revisión de revistas científicas internacionales, en idiomas inglés y español con el objetivo de describir la relación entre la seroprevalencia de T. gondii y el desarrollo de trastornos mentales en población adulta. Existe relación entre los trastornos mentales en la población adulta con la infección por Toxoplasma gondii y este aumenta la posibilidad de desarrollar esquizofrenia y depresión en individuos sin historial previo, y que podría exacerbar cuadros psiquiátricos previos con dificultad en el tratamiento. Sin embargo, no todos los datos estadísticos establecen una relación directa, algunos estudios demuestran una asociación, ciertos datos son discordantes, lo que abre una puerta para futuras investigaciones.
... Latent toxoplasmosis is can cause different behavioral and hormonal alteration in infected animals & humans and can contribute in causing various psychiatric and neurologic disorders (2). Infected rats and mice developed impaired coordination and performances of the motor neurons, defective learning & decreased avoidance of open predators & spaces (3). They are thought to be evolutionary mechanisms for increasing the chances of host that is ingested by feline (4). ...
Conference Paper
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This study included 115 pregnant women, the case group consisted of 65 women who were infected with toxoplasmosis, while the control group involved 50 pregnant women who were not infected with toxoplasmosis. All the studied women attended Baghdad teaching hospital during the period from 1st February 2021 to 1st March 2022. The results in the current study revealed NS. between the mean ages between the case group (41.84±15.88) years and the control group (40.85±15.48) years. There was HS. (P<0.01) in mean Toxoplasma IgM levels between the case group (2.00±1.17) and the control group (0.09±0.17), and there was also HS. (p<0.01) in mean Toxoplasma IgG levels between the case group (14.20±7.06) and the control group (0.06±0.11). The findings showed HS. (p<0.01) in serum zinc levels between the patients group (56.84±18.87) and the control group (88.09±14.85). The result also showed HS. (p<0.01) between the mean levels of T3 and TSH (3.16±1.44) and (2.63±1.06) respectively and the control groups (1.37±0.80) and (1.14±0.98) respectively, while NS. (p>0.05) was found between the levels of T4 (3.65±0.97) and the control group (4.02±1.60). There was a correlation between Toxoplasma IgM and serum zinc (22.515), T3 (4.753), T4 (9.261), and TSH (2.795) with HS. (P<0.01), and a correlation between Toxoplasma IgG and serum zinc (17.505), T3 (11.736), T4 (11.377) and TSH (12.878) with HS. (P<0.01)
... The reaction mixture was transferred to a measuring cell and the microparticles were magnetically captured on the surface of an electrode. Electrochemiluminescence immunoassay (ECLIA) was measured using photomultiplier and the concentration of testosterone was calculated using calibration curve (Zouei et al., 2018) Stereological study: Within 20 minutes after slaughter, the scrotum was incised and the paired testicular weight (TW) was recorded using a digital scale. Small pieces were taken from three regions (proximal, middle and distal) of the left testes; immediately fixed in formalin 10% solution, embedded in paraffin, sectioned at 5µm with rotary microtome and stained later with hematoxylin and eosin. ...
Article
Full-text available
Background Toxoplasma gondii (T. gondii) is a worldwide distributed protozoan parasite which has infected a wide range of warm-blooded animals and humans. The most common form of T. gondii infection is asymptomatic (latent); nevertheless, latent toxoplasmosis can induce various alterations of sex hormones, especially testosterone, in infected humans and animals. On the other hand, testosterone is involved in behavioral traits and reproductive functions in both sexes. Hence, the purpose of this systematic review is to summarize the available evidence regarding the association between T. gondii infection and testosterone alteration. Methods In the setting of a systematic review, an electronic search (any date to 10 January 2023) without language restrictions was performed using Science Direct, Web of Science, PubMed, Scopus, and Google Scholar. The PRISMA guidelines were followed. Following the initial search, a total of 12,306 titles and abstracts were screened initially; 12,281 were excluded due to the lack of eligibility criteria or duplication. Finally, 24 articles met the included criteria. A mean±standard deviation (SD) was calculated to assess the difference of testosterone between T. gondii positive and T. gondii negative humans. The possibility of publication bias was assessed using Egger’s regression. P-value < 0.05 was considered statistically significant. Results This systematic review identified 24 articles (18 studies in humans and six studies in animals). Most human studies (13 out of 19) reported an increased level of testosterone following latent toxoplasmosis in males, while three studies reported decreased levels and two studies reported an insignificant change. Eleven articles (seven datasets in males and seven datasets in females) were eligible to be included in the data synthesis. Based on the random-effects model, the pooled mean± SD of testosterone in T. gondii positive than T. gondii negative was increased by 0.73 and 0.55 units in males and females, respectively. The Egger’s regression did not detect a statistically significant publication bias in males and females (p = value = 0.95 and 0.71), respectively. Three studies in male animals (rats, mice, and spotted hyenas) and two studies in female animals (mice and spotted hyenas) reported a decline in testosterone in infected compared with non-infected animals. While, one study in female rats reported no significant changes of testosterone in infected than non-infected animals. Moreover, two studies in male rats reported an increased level of testosterone in infected than non-infected animals. Conclusions This study provides new insights about the association between T. gondii infection and testosterone alteration and identifies relevant data gaps that can inform and encourage further studies. The consequence of increased testosterone levels following T. gondii infection could partly be associated with increased sexual behavior and sexual transmission of the parasite. On the other hand, declining testosterone levels following T. gondii infection may be associated with male reproductive impairments, which were observed in T. gondii-infected humans and animals. Furthermore, these findings suggest the great need for more epidemiological and experimental investigations in depth to understand the relationship between T. gondii infection and testosterone alteration alongside with future consequences of testosterone alteration.
Article
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Toxoplasma gondii is a protozoan parasite capable of infecting any warm-blooded species and can increase risk-taking in intermediate hosts. Despite extensive laboratory research on the effects of T. gondii infection on behaviour, little is understood about the effects of toxoplasmosis on wild intermediate host behavior. Yellowstone National Park, Wyoming, USA, has a diverse carnivore community including gray wolves (Canis lupus) and cougars (Puma concolor), intermediate and definitive hosts of T. gondii, respectively. Here, we used 26 years of wolf behavioural, spatial, and serological data to show that wolf territory overlap with areas of high cougar density was an important predictor of infection. In addition, seropositive wolves were more likely to make high-risk decisions such as dispersing and becoming a pack leader, both factors critical to individual fitness and wolf vital rates. Due to the social hierarchy within a wolf pack, we hypothesize that the behavioural effects of toxoplasmosis may create a feedback loop that increases spatial overlap and disease transmission between wolves and cougars. These findings demonstrate that parasites have important implications for intermediate hosts, beyond acute infections, through behavioural impacts. Particularly in a social species, these impacts can surge beyond individuals to affect groups, populations, and even ecosystem processes.
Article
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In the current study, performance of electrochemiluminescence immunoassay (ECLIA) in detection of anti-toxoplasma IgG in human sera was compared with that of enzyme-linked immunosorbent assay (ELISA). Furthermore, performance of an in house Dot-ELISA in detection of anti-toxoplasma IgG was compared with that of ECLIA and ELISA. In total, 219 human sera were tested to detect anti-toxoplasma IgG using Dynex DS2® and Roche Cobas® e411 Automated Analyzers. Discordant results rechecked using immunofluorescence assay (IFA). Then, sera were used in an in house Dot-ELISA to assess toxoplasma-specific IgG. Of the 219 samples, two samples were found undetermined using ECLIA but reactive using ELISA. Using IFA, the two sera were reported unreactive. Furthermore, two samples were found reactive using ECLIA and unreactive using ELISA. These samples were reported reactive using IFA. The overall agreement for the two former methods was 98% (rZ0.98.1; P < 0.001). The intrinsic parameters calculated for in house Dot-ELISA included sensitivity of 79.5, specificity of 78.2, and accuracy of 78.9%, compared to ECLIA and ELISA. Positive and negative predictive values included 82.9 and 74.2%, respectively. A 100% sensitivity was found in in house Dot-ELISA for highly reactive sera in ECLIA and ELISA. ECLIA is appropriate for the first-line serological screening tests and can replace ELISA due to high speed, sensitivity, and specificity, particularly in large laboratories. Dot-ELISA is a rapid, sensitive, specific, cost-effective, user-friendly, and field-portable technique and hence can be used for screening toxoplasmosis, especially in rural fields or less equipped laboratories.
Article
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Background Natural polysaccharides such as chitosan (CS) are widely used as antimicrobial agents. In recent years, and considering that CS has a strong antimicrobial potential, interest has been focused on antimicrobial activity of chitosan nanoparticles (CS NPs). The main factors affecting the antibacterial activity of chitosan include molecular weight (MW) and concentration. In this regard, the aim of this study was to produce various MWs and concentrations of CS NPs, through the ionic gelation method, and investigate their potential anti-parasitic activity against tachyzoites of Toxoplasma gondii RH strain. Materials and methods The MWs and degree of deacetylation of the CS were characterized using viscometric and acid–base titration methods, respectively. The efficacy of various MWs and concentrations of NPs was assessed by performing in vitro experiments for tachyzoites of T. gondii RH strain, such as MTT assay, scanning electron microscopy, bioassay in mice and PCR. In vivo experiment was carried out in BALB/c mice which were inoculated with tachyzoites of T. gondii RH strain and treated with various MWs of CS NPs. Results The results of in vitro and in vivo experiments revealed that anti-Toxoplasma activity strengthened as the CS NPs concentration increased and the MW decreased. In vitro experiment showed 100% mortality of tachyzoites at 500 and 1,000 ppm concentrations of low molecular weight (LMW) CS NPs after 180 min and at 2,000 ppm after 120 min. Furthermore, a 100% mortality of tachyzoites was observed at 1,000 and 2,000 ppm concentrations of medium molecular weight (MMW) CS NPs and at 2,000 ppm concentration of high molecular weight (HMW) CS NPs after 180 min. Growth inhibition rates of tachyzoites in peritoneal exudates of mice receiving low, medium and high MWs of CS NPs were found to be 86%, 84% and 79% respectively, compared to those of mice in sulfadiazine treatment group (positive control). Conclusion Various MWs of CS NPs exhibited great anti-Toxoplasma efficiency against tachyzoites of RH strain, with the greatest efficacy shown by LMW CS NPs in both experiments. It seems that CS NPs can be used as an alternative natural medicine in the treatment of toxoplasmosis.
Article
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Here, we hypothesized that in chronic Toxoplasma gondii infection communication among immune cells promotes neuroinflammation through cytokine networks and potentiate cognitive impairments in BALB/c mice with Alzheimer's disease (AD). The animal model of Toxoplasma infection was established by the intraperitoneal inoculation of 20-25 tissue cysts from Tehran strain of T. gondii. We injected amyloid-beta 1-42 peptide (A1-42, 1 and 2 µL) into the hippocampus of BALB/c mice to establish an animal model of AD. The behavioral experiments such as spatial learning and memory were performed using Morris water maze test. The mRNA levels of TNF-, IL-1, IFN-, and inducible nitric oxide synthase (iNOS) were examined by real-time PCR. We found that T. gondii infection caused AD-like symptoms and impaired learning and memory functions of the infected BALB/c mice. We also found that in Toxoplasma infection + A1-42 (1 µL) group, T. gondii infection could potentiate AD in infected mice receiving sub-dose of A1-42 (1 µL) and caused considerable impairment in learning and memory functions similar to AD group. Comparison of the results demonstrated that mRNA levels of IL-1, TNF-, IFN-, and also iNOS significantly (P < 0.001) increased in T. gondii + A1-42 (1 µL) in comparison with the other tested groups. The obtained results showed that chronic T. gondii infection communication among immune cells promotes neuroinflammation through cytokine networks and induce pathological progression of AD in the mice brain, whereas, neuroanatomical Toxoplasma tissue cysts presence in the brain could also affect the behavioral functions in T. gondii infected mice.
Article
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There are conflicting reports concerning the association of Toxoplasma gondii infection with increased risk of mental disorders. This investigation will provide a good understanding about defining the possible association between T. gondii exposure and risk of anxiety and cognitive alterations. Besides, a secondary objective of this study was to determine the effect of pioglitazone administration on the possible alterations induced by T. gondii exposure. Male BALB/c mice were used for this study. The animal model of Toxoplasma infection was established by the intraperitoneal inoculation of 20-25 tissue cysts from Tehran strain of T. gondii. Pioglitazone (20 mg/kg, i.p.1/day) was administered to the animals for 2 weeks before behavioural tests. Behavioural tests including open-field, elevated plus-maze and passive avoidance learning were evaluated in the groups. Since cytokines were implicated as a contributing factor for mood disorders, the mRNA levels of TNF-α, IL-1β, IL-6 as well as inducible nitric oxide synthase (iNOs) were examined by real-time PCR. Findings demonstrated that T. gondii caused anxiety-like symptoms and impaired cognitive functions of the infected BALB/c mice, whereas pioglitazone, a peroxisome proliferator-activated receptor agonist, showed a promising effect against the cognitive impairments induced by Toxoplasma infection. The results also revealed that the mRNA levels of the aforementioned cytokines were significantly (p < 0.05) increased in the infected mice compared to the uninfected BALB/c ones. Pioglitazone can be offered as a potential neuroprotective agent in the treatment of patients with T. gondii infection that manifests anxiety and cognitive impairments; however, further studies are needed to clarify the exact mechanisms.
Article
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We hypothesized that in Toxoplasma gondii infection, communication among immune cells promotes neuroinflammation through cytokine networks and induces pain sensitivity under conditions of neuropathic pain. The animal model of Toxoplasma infection was established by the intraperitoneal inoculation of 20-25 tissue cysts from Tehran strain of T. gondii to BALB/c mice. Amitriptyline (20 mg/kg, i.p., 1/day) administrated to animals for 7 days before behavioral tests. Pain behavioral tests including tail flick, hot plate, and formalin test were evaluated in all the groups. The mRNA levels of tumor necrosis factor (TNF)-α, interleukin (IL)-1β, and IL-6 were examined by real-time PCR. Results revealed that T. gondii induce hyperalgesia in the infected mice, whereas amitriptyline showed a promising effect against the hyperalgesia induced by Toxoplasma infection. The mRNA levels of the aforementioned cytokines significantly (P < 0.05) increased in the infected mice compared to the uninfected ones. Obtained findings suggested that T. gondii infection could promote neuroinflammation through cytokine networks and induced hyperalgesia in BALB/c mice, whereas amitriptyline as an analgesic drug reverses them.
Article
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Toxoplasma gondii is a unique intracellular parasite, which infect a large proportion of the world population, but uncommonly causes clinically significant disease. The present study was performed to estimate the prevalence of toxoplasmosis in 400 apparently healthy blood donor males, their ages were between 18 and 57 years using enzyme linked immunosorbent assay, and to examine the effects of infection on total testosterone, free testosterone and follicle stimulating hormone (FSH) levels in their sera. Seroprevalence showed 10 (2.5 %) and 121 (30 %) of them had IgM and IgG antibodies respectively. Both acute and chronic toxoplasmosis in males recorded higher significant (P < 0.05) mean concentration for total and free testosterone hormone, they were 12.188 ± 0.73, 7.837 ± 0.52 ng/ml and 44.121 ± 1.76, 27.984 ± 0.94 pg/ml respectively. The mean concentration of FSH revealed non-significant (P < 0.05) differences in both disease activities, they were 6.41 ± 0.47 and 6.515 ± 0.51 IU/ml respectively.
Article
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Toxoplasma gondii is an intracellular protozoan parasite that infects human and animals. Toxoplasma parasites are isolated from different parts of animals even from semen but there are little information about the effect of toxoplasmosis on fertility in animals and humans. In present study, the effect of chronic toxoplasmosis on serum levels of testosterone in men was studied. In this case-control study, 1026 men referred to Arak Post Marriage Center were selected. Three ml of blood samples were collected and sera separated by centrifugation at room temperature. These sera were analyzed for detection of anti-T. gondii IgG antibody. Next 365 positive sera were selected as cases and also the same number of negative sera (365) as controls. Finally the level of testosterone was analyzed for the cases and controls samples. Serological tests on the sera of 1,026 men in Arak City showed that 365 of them had anti-Toxoplasma antibody. Comparison of testosterone concentration in case and control groups showed that testosterone concentration in case group was less than control group and this difference was statistically significant (P<0.05). The chronic toxoplasmosis could affect reproductive parameters in men.
Book
Found worldwide from Alaska to Australasia, Toxoplasma gondii knows no geographic boundaries. The protozoan is the source of one of the most common parasitic infections in humans, livestock, companion animals, and wildlife, and has gained notoriety with its inclusion on the list of potential bioterrorism microbes. In the two decades since the publication of the first edition of Toxoplasmosis of Animals and Humans there has been an explosion of knowledge concerning T. gondii and toxoplasmosis. Still used extensively as a cell model, its genome has recently been published making it a subject of even greater scientific interest. Keeping the organizational style that made the previous edition so popular and usable, this second edition has been completely revised and updated. New in the Second Edition: Expanded information on the cultivation, maintenance, and preservation of T. gondii Expanded information on the cell biology and molecular biology of the parasite Reviews all literature from the past 20 years for each domestic animal Summarizes information on the worldwide prevalence of toxoplasmosis in pregnant women and the devastating disease it can cause in newborn Written by one of the pioneers of the field, the book provides unique information on all known host types for this parasite. It distills the voluminous and potentially confusing scientific literature that has grown geometrically in the 20 years since the publication of the first edition into a comprehensive resource. The single author approach ensures a strong foundation in the biology and a seamless integration of topics. The new edition of this groundbreaking work is the only volume to cover toxoplasmosis of animals and humans thoroughly in one source. It supplies an entry point to further research by cutting through the morass of literature to identify the most relevant references.
Article
Introduction and objective: Toxoplasma gondii is an intra cellular protozoan parasite which infects 30 to 60% of the world population. A wide range of toxoplasmosis conditions has been studied, but there are still unknown damages which must be explored. In the present research, the effect of this parasite on testosterone and cortisol changes in the infected men and women was examined. Materials and methods: A total of 180 patients (73 females and 107 males), were examined for lgG anti-Toxoplasma antibody, cortisol and testosterone in their plasma. In addition, the patients also filled in personality questionnaire DASS21 (depression, anxiety, and stress). Results: Results showed that 24(%13/33) females and 39(%20) males were positive with lgG anti-Toxoplasma antibody, respectively. A statistically significant correlation between Toxoplasma infection and testosterone and cortisol increase in women and men were observed. Stress and anxiety index also increased in men and women whereas depression index increased only in men. Conclusion: The results show a direct relation between raise Toxoplasma infection and cortisol, and testosterone increase in bout men and women and high DASS21 test score in Toxoplasma infected group. Significance and impact of the study: Our results may indicate that following Toxoplasma infection, the probability of stressful condition is high.