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Augustana College

Toxoplasma gondii as a Potential Risk Factor for Paranoid, Disorganized, and Catatonic

Schizophrenia

Taylor SmithMicrobes in Action Senior Inquiry BIOL464

Dr. Kimberly Murphy25 January 2016

Taylor Smith

Senior Inquiry

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Dr. Kimberly Murphy

12 February 2016

Toxoplasma gondii as a Potential Risk Factor for Different Classifications of

Schizophrenia

Abstract

The complex psychophysiology of schizophrenia makes it extremely

difficult to understand. Its relationship to certain microbes has been shown

through previous research, however no significant data has been found. This

study aimed to determine the association between exposure to the parasite,

Toxoplasma gondii (T. gondii), and the risk of paranoid schizophrenia,

disorganized schizophrenia and/or catatonic schizophrenia. Sera were tested

for IgG antibody levels in patients diagnosed with the three different

classifications of schizophrenia as well as control patients. This research has

potential to have great implications as far as prevention and treatment

strategies for schizophrenia disorder.

Background and Significance

There is a lack of knowledge surrounding the factors linked to the

development of schizophrenia, and because schizophrenia has such a

complex psychophysiology, the disorder has been very poorly understood for

quite some time. However, the discovery of the connection between gut

microbes and the brain sparked interest in the minds of neuroscientists, and

possible links between microbes and various neurological disorders and

diseases are being discovered.

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Preliminary research on a possible connection between T. gondii and

the development of schizophrenia has been conflicting. On one hand, a study

performed by Hamidinejat et al. concluded that exposure to T. gondii, an

intracellular parasitic protozoan, is a potential risk factor for schizophrenia

(Hamidinejat et al. 2010). On the other hand, Saraei-Sahnesarael et al.

conducted a study that found no association between schizophrenia and

infection with T. gondii (Saraei-Sahnesaraei et al. 2009). Yolken et al. studied

antibodies to T. gondii in patients undergoing their first schizophrenic

episode, and by using ELISA and Western blotting techniques, found

significantly increased levels of the antibodies when compared to control

patients. Similar to the study done by Hamidinejat et al., Yolken et al.

determined a correlation between T. gondii and schizophrenia (Yolken et al.

2001). Finally, Conejero-Goldberg et al. conducted a study on postmortem

orbital frontal brain samples of patients with schizophrenia and the presence

of T. gondii. They did not detect any amount of T. gondii in the postmortem

brains, leading them to believe that viruses and protozoa may not be

involved in the development of schizophrenia (Conejero-Goldberg et al.

2003).

So far, there has been no significant data found in terms of exposure to

T. gondii and the development of schizophrenia, just support in terms of the

hypothesis stating the two might be linked, and correlation does not define

causation. It is known, however, that patients with schizophrenia have been

found to have significantly increased levels of T. gondii antibodies when

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compared to healthy control patients (Hamidinejat et al. 2010). Despite this

previous research, little has been done in terms of researching the parasite

and its link to specific classifications of schizophrenia as opposed to

schizophrenia in general. A study conducted in Durango City, Mexico found

that the prevalence of infection with T. gondii was significantly higher in

patients with simple schizophrenia than those with paranoid schizophrenia,

but no significant conclusions can be drawn from their data in terms of the

other classifications of schizophrenia (Alvarado-Esquivel et al. 2011). This

study will aim to determine the association between exposure to the parasite

T. gondii and the risk of paranoid schizophrenia, disorganized schizophrenia

and/or catatonic schizophrenia.

Toxoplasma gondii (T. gondii)

T. gondii is a parasite with a strong affinity for brain tissue (Zhu 2009)

that can cause persistent infection in both humans and other warm-blooded

mammals (Hamidinejat et al. 2010). Felids (cats) are the most common host

for this parasite and can infect humans in three different ways. These forms

of infection include consumption of raw or undercooked meat containing

tissue cysts, ingestion of water or fruits and vegetables contaminated with

oocysts from the fecal matter of infected cats, and lastly, can be transmitted

congenitally. A previous study by Mortensen et al. looked at infectious

agents, including T. gondii, and their effect on a developing fetus, newborn,

or young child. They found a significant relationship between increased

antibody levels in newborn children and being diagnosed with schizophrenia

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before the age of 18 (Mortensen et al. 2007). This parasite also has the

ability to change its behavior and its host’s behavior to increase its

transmission (Khademvatan et al. 2014). T. gondii infections can vary from

mild to severe, including serious issues with the lymph nodes, eyes, and

central nervous system (Alvarado-Esquivel et al. 2010). In majority of cases,

T. gondii stays dormant in adults and causes no issues, but infection has

shown to lead to neurological and/or psychiatric symptoms in some cases

(Hamidinejat et al. 2010, Zhu 2009). Toxoplasmosis is the resulting disease

of infection with T. gondii. Mothers that become infected with T. gondii

during early stages of pregnancy most likely give birth to babies with

multisystem disease. These children can suffer from severe neurological

issues such as mental retardation, hydrocephaly and microcephaly

(Mortensen et al 2007, Yolken et al. 2001). In certain animals, past research

has shown that infection with T. gondii can lead to changes in behavior and

neurotransmitter levels that are associated with the pathogenesis of

schizophrenia (Yolken et al. 2001). Many anti-psychotic and mood-stabilizing

drugs, such as Haloperidol and valproic acid, are used in the treatment of

schizophrenia, and these drugs are known to prevent the development of T.

gondii-associated changes in behavior and brain function (Khademvatan et

al. 2014). T. gondii is a very common parasite among warm-blooded animals,

and therefore research that tests its effects on humans is very beneficial

(Khademvatan et al. 2014).

Schizophrenia

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Schizophrenia can be characterized as a disorder of abnormal brain

connectivity. This abnormal connectivity leads to increased functional

connectivity (Fornito et al. 2015). It is categorized by a variety of social

and/or occupational dysfunctions (American Psychiatric Association 2000).

The symptoms associated with schizophrenia include affective flattening,

alogia and avolition. Affective flattening occurs when a patient’s face

appears to be immobile and/or unresponsive. These patients also have a

hard time maintaining eye contact and using their body language. (American

Psychiatric Association 2000). Alogia is the “poverty of speech”, and causes

patients to have a decreased sentence fluency and diminution of thoughts

and production of speech. Lastly, avolition is the inability to participate and

continue to participate in organized activities. Patients that suffer from

avolition may sit in silent isolation for hours at a time, choosing not to

participate in any sort of activity (American Psychiatry Association 2000).

Schizophrenia affects the way a person thinks, feels and acts. Some

patients diagnosed with schizophrenia have a hard time telling what is real

and what is imaginary in everyday life. People suffering from schizophrenia

may be socially withdrawn, have difficulty expressing emotions, and may be

violent or have multiple personalities. Factors such as genes, diet and

environment are thought to play a role in the development of the disorder

(Fornito et al. 2015, Hamidinejat et al. 2010). From past research, it seems

like schizophrenia tends to run in families and can be linked to certain viral

infections or high stress situations (Yolken et al. 2001). Schizophrenia

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appears in patients when they are going through hormonal and physical

changes and may present as an imbalance of certain chemicals of the brain

such as serotonin and dopamine. It has been shown from previous research

that dopamine is one of the main chemicals associated with psychosis such

as schizophrenia in patients with toxoplasmosis (Zhu 2009). Early treatment

is best in terms of effectiveness; schizophrenia can be treated by means of

rehabilitation programs, support groups, therapy and counseling. There are

also a few antipsychotic medications that can be used to try to manage the

disorder, however, side effects are wearing and common (Fornito et al.

2015).

The three most common classifications of schizophrenia are paranoid

schizophrenia, disorganized schizophrenia, and catatonic schizophrenia

(Schennach et al. 2012). Paranoid schizophrenia can be characterized by

feelings of suspicion, persecution, or a combination of emotions similar to

those of paranoia (Witkowska 2015). Disorganized schizophrenics are

incoherent in speech and thought, but these patients do not always have

delusions (Fukunaga et al. 2013). Lastly, catatonic schizophrenia causes the

patient to be negative and withdrawn (Waris et al. 2014). The other

classifications of schizophrenia include residual schizophrenia and

schizoaffective disorder. Residual schizophrenia occurs when the patient is

no longer experiencing delusions, but also no longer has a motivation for life.

Schizoaffective disorder takes place when a patient suffers from

schizophrenia and another major depressive disorder such as depression or

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bipolar disorder. Although residual schizophrenia and schizoaffective

disorder are classifications of schizophrenia, this study focused on the three

main classifications including paranoid, disorganized, and catatonic

schizophrenia. Understanding the relationship between these three

classifications and T. gondii could be very helpful in terms of prevention and

treatment strategies as well.

Paranoid Schizophrenia

Paranoid schizophrenia can be characterized by feelings of suspicion,

persecution, or a combination of emotions similar to those of paranoia

(Witkowska 2015). Patients with paranoid schizophrenia have great delusions

and auditory hallucinations that are usually persecutory. Symptoms that are

characteristic of catatonic schizophrenia are not present in a paranoid

schizophrenic. Their hallucinations and delusions are usually of the same

theme, and associated issues include anxiety and anger. These patients

usually have capacity for independent living and symptoms have been found

to become more stable over time (American Psychiatric Association 2000).

Disorganized Schizophrenia

Disorganized schizophrenia is possibly the most difficult classification

to diagnose and understand because disorganized schizophrenics are

incoherent in speech and thought, but these patients do not always have

delusions (Fukunaga et al. 2013). Individuals with this type of schizophrenia

may lose their train of thought easily, have completely unrelated answers for

the questions they are asked, and may have mildly to severely impaired

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speech. Their symptoms are usually persistent with no stability over time

(American Psychiatric Association 2000).

Catatonic Schizophrenia

Lastly, catatonic schizophrenia causes the patient to be negative and

withdrawn (Waris et al. 2014). Catatonic behavior involves a decrease in

reactivity to the environment, childlike silliness, agitation, and trouble with

activities of daily living such as making dinner or brushing one’s teeth. These

patients need to be watched closely so that they do not cause harm to

themselves or others. They often mimic others that are speaking and can be

extremely “high” and “low” in terms of emotions. (American Psychiatric

Association 2000). Understanding the relationship between these three

classifications and T. gondii could be very helpful in terms of prevention and

treatment strategies.

Research Design and Methods

Patients diagnosed with schizophrenia, as well as control patients with

healthy brains, were gathered for this experiment. Gender was noted for

each patient as it is a factor that seems to play a role in the development of

schizophrenia (Khademvatan et al. 2014). Residence, marital status, level of

education and ethnicity were not noted, as previous studies have shown

there to be no connection between those areas of demographic information

and the development of schizophrenia in relation to T. gondii (Khademvatan

et al. 2014). The patients were divided into groups according to their

classification of either paranoid, disorganized, or catatonic schizophrenia.

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The samples were blindly tested so that person performing the experiment

would not know the identity of the patient.

Demographic Patient Information

This study was conducted in China. Worldwide, the prevalence rate for

schizophrenia is about 1.1% of the population over eighteen years old, and

because China has such a large population, it can be concluded that there

would be approximately 6-12 million people in China diagnosed with

schizophrenia, allowing a bigger sample size. This study tested the sera of

500 patients diagnosed with schizophrenia. 250 of the patients were male,

while the other 250 were female. This study also tested the sera of 500

control patients with the same gender ratio. All patients gave informed

consent before their participation in the experiment.

Patient Diagnosis

All diagnoses were made using the Diagnostic and Statistical Manual of

Mental Disorders (DMS). None of the patients used in this research were

immune-deficient or diagnosed with another neurological disorder or

disease.

Serological Tests

All samples were centrifuged for 20 minutes and stored at -20°C.

Blood samples (5mL) were taken from patients and levels of T. gondii

antibodies were recorded by means of an enzyme-linked immunosorbent

assay (ELISA), which is a test that detects antibodies in the blood

(Khademvatan et al. 2014). It is used to determine whether a sample has

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antibodies present that relate to certain infections, such as T. gondii. The

antibodies are proteins that are produced in a patient’s body to prevent

antigens from attacking the body. When the blood sample has antibodies

present, the antibody attaches to the antigen and a color change occurs,

indicating their presence. This method was used in this experiment because

a strategy was needed to test the T. gondii antibody levels of all of the

patients that participated.

Statistical Tests

Results will be analyzed using Fisher’s exact test, a statistical

significance test. P-values that are less than or equal to 0.05 will be

considered statistically significant (Khademvatan et al. 2014).

Potential Outcomes and Benefits of Research

In terms of addressing and obtaining an answer to this research

question, a lot is at stake in terms of science and treatment of schizophrenia.

This research is significant because latent infection of T. gondii is actually

quite common in humans, and toxoplasmosis is known to be associated with

a variety of different neurological disorders that result in psychosis, not just

schizophrenia. If we can find a connection to schizophrenia, there is

possibility of the discovery of a better way to diagnose, treat and possibly

prevent schizophrenia.

This information would benefit a wide range of people including

doctors, psychiatrists, psychologists, researchers, and patients and their

loved ones affected by schizophrenia. A study conducted in 2008 focused on

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the effects of caring for someone with schizophrenia can have on a

caregiver. Burden of care can be defined as impacts and consequences that

a caregiver goes through as a result of taking care of a patient with a certain

disorder or disease. Burden of care can lead to many problems, such as

emotional, psychological, physical and economic issues. It can also result in

shame, embarrassment and feelings of guilt (Awad et al. 2008). Hopefully,

with the help of T. gondii and schizophrenia research, the incidence of both

schizophrenic patients and exhausted caregivers will slowly fall. Many other

infections including herpes simplex, rubella, polio, and varicella zoster virus

have been found to possibly contribute to the development of schizophrenia

(Hamidinejat et al. 2010). These viruses could be the center of very

important future research concerning schizophrenia and its development.

This research could also lead to inquiries involving other microbes and their

links to various diseases and disorders, specifically neurological issues.

Potential outcomes of this research could include a few different

findings. One potential outcome would be a significance in T. gondii

antibodies for the 20-29 age group, as shown in Table 4. This would be

expected because schizophrenic patients tend to start showing symptoms

around the ages of 20-25. Another potential outcome would be a significance

in T. gondii antibodies among women participants as shown in Table 2. This

would be expected because of previous research that has been conducted.

Khademvatan et al. showed through their research that there was a

significant relationship between female schizophrenic patients and levels of

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T. gondii antibodies (Khademvatan et al. 2014). There could be significance

found among one specific classification of schizophrenia, leading us to

believe that infection with T. gondii plays a bigger role in the development of

that specific classification as opposed to any other classification. Another

potential outcome could include all classifications of schizophrenia showing

the same amount of significance in terms of antibody levels as shown in

Table 3. All patients with schizophrenia would show significant levels of T.

gondii antibodies as shown in all of the tables generated from this

experiment.

One major drawback in terms of this study is that schizophrenia is

thought to be linked to a wide variety of different problems and experiences,

and this research proposal solely examines the role of T gondii in terms of

the development of the disorder. All other potential risk factors of

schizophrenia should be examined and researched as well. T. gondii is also a

very common parasite and is knowingly linked to several different disorders

and diseases, which complicates the research by lessening the amount of

variable control. Another complication is the limitation in terms of sample

size since schizophrenia is such a rare disorder and only affects 1% of the

population. Lastly, future researchers will run into the ethical complication of

being not able to infect a patient with T. gondii to observe the outcome. This

would be a beneficial research strategy, however, our ethical standards as a

society forbid that sort of testing and intentional exposure to infectious

agents.

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The next step in this research is to determine whether the association

between T. gondii and schizophrenia is due to a causal relationship between

the two, an increased risk of T. gondii infection for patients with

schizophrenia, or another reason that hasn’t been uncovered (Alvarado-

Esquivel et al. 2001). Other areas of research could include comparing IgG

antibody levels of out-patients with schizophrenia and patients with

schizophrenia that are going through their first episode (Alvarado-Esquivel et

al. 2001). It may also be beneficial to study the different genotypes of T.

gondii and their relationship to schizophrenia (Khademvatan et al. 2014).

There have been additional neurological disorders that have been found to

be associated with T. gondii infection, such as bipolar disorder (Yolken et al.

2006). Despite treatment, bipolar disorder is a recurring chronic disorder

that can be characterized by extreme mood swings, depression, and in some

cases suicidal tendencies. The underlying cause of this disorder has not yet

been recognized, although genetic and neurobiological factors seem to play

a role (Koenders et al. 2015). It would be beneficial to research this disorder

and its relationship to T. gondii to see if it is significant. It would also be

beneficial to study all of the course types of bipolar disorder and their

relationship to the infection as well (Koenders et al. 2015). Lastly, it could be

beneficial to research the incubation period of T. gondii, and whether or not

there is a relationship between the time period between infection with T.

gondii and the onset of schizophrenia (Alvarado-Esquivel et al. 2001).

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Past research has shown a correlation between patients developing

schizophrenia and their exposure to cats during their childhood years which

could also be an area of future research (Hamidinejat et al. 2010). This could

be done by exploring the relationship between infection with T. gondii,

schizophrenia, and exposure to cats between the ages of 0-35. Testing this

relationship would be beneficial because it is already known that the most

common hosts of T. gondii are cats.

A strong genetic component in terms of the risk of developing

schizophrenia has been found through family and twin studies, which could

be another area of further research. A recent study from 2015 showed that a

certain complement pathway of the brain occurs frequently in schizophrenia.

A gene, called the complement 3 (C3) gene has been known to play a big

role in the processes of complement pathway activation. This provides

evidence that the C3 gene is possibly involved in the development of

schizophrenia, causing genetics to be a major factor in this disorder (Ni et al.

2015). It has also been found that schizophrenia can be associated with

environmental factors, which could be important research in terms of

preventing the development of the disorder (Yolken et al. 2001).

In terms of interdisciplinary research, a lot can be said about how this

research could positively affect suicide rates and cost to society. First, there

has been a close relationship identified between schizophrenia and suicide.

Most suicides due to schizophrenia happen when the patient is experiencing

the worst of their symptoms, and suicidal drive has been found to be one of

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the most severe symptoms among schizophrenic patients. It has been noted

that approximately 2-12% of suicides are linked to schizophrenia. Popovic et

al. aimed to research the possible risk factors surrounding suicide and

schizophrenia. Depression, history of suicide attempt, number of psychiatric

admissions, hopelessness, age, closeness of illness onset, gender, hospital

admissions and substance misuse were all reported as risk factors for suicide

for schizophrenic patients. (Popovic et al. 2014). Research on T. gondii in

relation to schizophrenia could help reduce suicide rates, which would

benefit society greatly by improving the mental health of people around the

world. Lastly, this research could have positive implications in terms of the

cost to society. Schizophrenia negatively affects society in terms of disease

management, death rates and financial costs. Disease management affects

not only schizophrenia patients, but caregivers, relatives, neighbors and

other people that come in contact with a schizophrenic patient in their daily

lives. Society also experiences a high death rate in terms of schizophrenia,

and has to cope with the resulting negative effects. This high death rate is

contributed to suicide, long-lasting negative health choices, metabolic

disorders and cardiovascular disease. Lastly, there are major financial costs

to society as a result of schizophrenic patients that could be avoided if better

treatment and prevention strategies were in place. Between potential for

institutionalization and chronic use of treatments, schizophrenia costs

society a lot of money, which could be resolved by discovering more about

this this disorder and its relationship to T. gondii (Millier et al. 2014).

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Conclusion

Mental illness is a growing problem and is poorly understood compared

to what is known about other diseases that are more frequently researched.

This research has the potential to help many people and gain knowledge

about schizophrenia, a disorder that very little is known about. Not only

would this study aid in learning about schizophrenia in general, but it is

unique in the way that it targets the different classifications of schizophrenia

as well. Conclusions could be drawn in terms of the way this parasite is

involved in the development of schizophrenia, which would benefit the

research in terms of the gut-brain relationship.

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Tables, Figure Legends, and Figures

Table 1 Patient

Demographics

Feature Paranoid Disorganized Catatonic Control TotalT.gondii Positive 63 55 71 138 327Negative 113 96 102 362 673GenderMale 82 83 85 250 500Female 85 82 83 250 500Age<20 51 53 43 54 20120-29 54 43 51 49 19730-39 49 54 49 53 20540-49 53 51 53 51 208>50 43 49 54 43 189

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Table 2 Anti-T. gondii Antibodies in Patients with Schizophrenia and Control

Group

Gender Paranoid Disorganized Catatonic ControlSignificance

Male 27/82 31/83 25/85 66/250 0.3Female 42/85 44/82 39/83 72/250 0.001

Paranoid Male

Paranoid Female

Disorganized Male

Disorganized Female

Catatonic Male

Catatonic Female Significance

IgG-positive 27/82 42/85 31/83 44/82 25/85 39/83 0.009

Table 3 Latent Toxoplasmosis in Patients with Schizophrenia

Table 4 Latent Toxoplasmosis According to Age in Patients with

Schizophrenia and Control Group

Age Paranoid Disorganized Catatonic Control Significance <20 0 0 0 19/54 20-29 27/54 20/43 25/51 14/49 0.00130-39 16/49 18/54 16/49 19/53 0.740-49 18/53 16/51 19/53 16/51 0.7>50 13/43 14/49 19/54 13/43 0.7