Research Article
BibTex RIS Cite

THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS

Year 2019, Volume: 14 Issue: 1, 33 - 45, 31.01.2019

Abstract

      Toxoplasma Gondii is
a zoonotic parasite showing intracellular localization. Although it doesn’t
select a specific region in the brain tissue, the cyst forms occurring in the
chronic phase may cause behavioral changes when it is located in the brain
regions related to behavior. The aim of this study is to investigate whether
there is a relationship between neurodegenerative and neuropsychiatric diseases
caused by antibodies transmitted to the first generation of T.Gondii infection
by behavioral tests. In this study, using a total of 24 female and 6 male rats.
Behavioral tests have been applied to F1 generation groups female and male. In
this study, female rats with chronic T.Gondii infection have been found to have
increased anxiety in open field in the first generation male offsprings and
decreased locomotor activity. Increased mobility in male offsprings has been
observed in the elevated plus maze test. In female offspring, it has reduced
anxiety and depression. 

References

  • 1. Arling, T.A., Yolken, R.H., Lapidus, M., Langenberg, P., Dickerson, F.B., Zimmerman, S.A., Balis, T., Cabassa, J.A., Scrandis, D.A., and Tonelli, L.H., (2009). Toxoplasma Gondii Antibody Titers and History of Suicide Attempts in Patients with Recurrent Mood Disorders. The Journal of nervous and mental disease 3(12):905-908.
  • 2. Brown, R.G., Landau, S., Hindle, J.V., Playfer, J., Samuel, M., Wilson, K.C., Hurt, C.S., Anderson, R.J., Carnell, J., and Dickinson, L., (2011). Depression and Anxiety Related Subtypes in Parkinson's Disease. Journal of Neurology, Neurosurgery & Psychiatry: jnnp. 2010.213652.
  • 3. Buentello, E., (1958). Preliminar Observations on the Relationship between Toxoplasmosis, Lysergic Acid and Schizophrenia.Gaceta medica de Mexico 88(10): 693-708.
  • 4. Caiaffa, W.T., Chiari, C.A., Figueiredo, A.R., Orefice, F., and Antunes, C.M., (1993). Toxoplasmosis and Mental Retardation: Report of a Case-Control Study. Memórias do Instituto Oswaldo Cruz 88(2): 253-261.
  • 5. Chorlton, S.D., (2017). Toxoplasma Gondii and Schizophrenia: a Review of Published RCTs. Parasitology Research: 1-7.
  • 6. Dodson, R.B., Rozance, P.J., Fleenor, B.S., Petrash, C.C., Shoemaker, L.G., Hunter, K.S., and Ferguson, V.L., (2013). Increased Arterial Stiffness and Extracellular Matrix Reorganization in Intrauterine Growth-Restricted Fetal Sheep. Pediatr Res 73(2):147-154.
  • 7. Dubey, J. and Jones, J., (2008). Toxoplasma Gondii Infection in Humans and Animals in The United States. International journal for parasitology 38(11): 1257-1278.
  • 8. Duryea, E., Nicholson, F., Cooper, S., Roberts, S., Rogers, V., McIntire, D., Sheffield, J., and Stewart R., (2015). The Use of Protease Inhibitors in Pregnancy: Maternal and Fetal Considerations. Infect Dis Obstet Gynecol 2015: 563727.
  • 9. Flegr, J., (2013). How and Why Toxoplasma Makes us Crazy. Trends in parasitology 29(4): 156-163.
  • 10. Flegr, J., Lenochová, P., Hodný, Z., and Vondrová, M., (2011). Fatal Attraction Phenomenon in Humans–Cat Odour Attractiveness Increased for Toxoplasma-Infected Men While Decreased for Infected Women. PLoS neglected tropical diseases 5(11): e1389.
  • 11. Guimarães, R.A., Asth, L., Engelberth, R. C., Souza de, J., Cavalcante, de Paula Soares-Rachetti, V., and Gavioli, E.C., (2015). Spontaneous Failure of the Estrous Eycle Induces Anxiogenic-Related Behaviors in Middle-Aged Female Mice. Physiology & behavior 147: 319-323.
  • 12. Harker, K., Ueno, N., and Lodoen, M., (2015).Toxoplasma Gondii Dissemination: a Parasite's Journey Through the Infected Host. Parasite immunology 37(3): 141-149.
  • 13. Jiao, F., Zhang, D., Jiang, M., Mi,J., Liu, X., Zhang, H., Hu, Z., Xu, X., and Hu, X., (2017). Label-Free Proteomic Analysis of Placental Proteins During Toxoplasma Gondii Infection.Journal of proteomics 150: 31-39.
  • 14. Kaur, A., Jindal, S., Kaur, I., and Chopra, K., (2013). Effect of Sesamol on the Pathophysiological Changes Induced by Surgical Menopause in Rodents.Climacteric 16(4):426-437.
  • 15. Khan, A., Dubey, J., Su, C., Ajioka, J.W., Rosenthal, B.M., and Sibley, L.D., (2011). Genetic Analyses of a Typical Toxoplasma Gondii Strains Reveal a Fourth Clonal Lineage in North America. International journal for parasitology 41(6): 645-655.
  • 16. Kusbeci, O.Y., Miman, O., Yaman, M., Aktepe, O.C., and Yazar, S., (2011). Could Toxoplasma Gondii Have Any Role in Alzheimer Disease? Alzheimer Disease & Associated Disorders 25(1):1-3.
  • 17. Liu, X., Zhao, M., Yang, X., Han, M., Xu, X., Jiang Y., and Hu,X., (2014). Toxoplasma Gondii Infection of Decidual CD1C+ Dendritic Cells Enhances Cytotoxicity of Decidual Natural Killer Cells. Inflammation 37(4):1261-1270.
  • 18. Liu, Y., Zhao, M., Xu, X., Liu, X., Zhang, H., Jiang, Y., Zhang, L., and Hu, X., (2014). Adoptive Transfer of Treg Cells Counters Adverse Effects of Toxoplasma Gondii Infection on Pregnancy.The Journal of infectious diseases, 210(9):1435-1443.
  • 19. Miman, O., Kusbeci, O.Y., Aktepe, O.C., and Cetinkaya, Z., (2010). The Probable Relation between Toxoplasma Gondii and Parkinson's Disease. Neuroscience letters 475(3):129-131.
  • 20. Misslin, R., (2003). The Defense System of Fear: Behavior and Neurocircuitry. Neurophysiologie Clinique/Clinical Neurophysiology, 33(2):55-66.
  • 21. Montoya, J.G. and Liesenfeld, O., (2004). Toxoplasmosis. Lancet 363(9425):1965-1976.
  • 22. Notarangelo, F., Wilson, E., Horning, K., Thomas, M., Harris, T., Fang, Q., Hunter, C., and Schwarcz, R., (2014). Evaluation of Kynurenine Pathway Metabolism in Toxoplasma Gondii-Infected Mice: Implications for Schizophrenia. Schizophrenia Research 152(1):261-267.
  • 23. Novotná, M., Havlíček,J., Smith, A. P., Kolbeková, P., Skallová, A., Klose, J., Gašová, Z., Písačka, M., Sechovská M., and Flegr, J. (2008). Toxoplasma and Reaction Time: Role of Toxoplasmosis in the Origin, Preservation and Geographical Distribution of Rh Blood Group Polymorphism.Parasitology, 135(11):1253-1261.
  • 24. Prandota, J., (2011). Metabolic, İmmune, Epigenetic, Endocrine and Phenotypic Abnormalities Found in Individuals With Autism Spectrum Disorders, Down Syndrome and Alzheimer Disease May be Caused by Congenital and/or Acquired Chronic Cerebral Toxoplasmosis.Research in Autism Spectrum Disorders 5(1):14-59.
  • 25. Ribeiro, D., Pereira, P., Machado, J., Silva, S., Pessoa, A., and Salvadori, D.M.F., (2004). Does Toxoplasmosis Cause DNA Damage? An Evaluation in Isogenic Mice under Normal Diet or Dietary Restriction. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 559(1):169-176.
  • 26. Rorman, E., Zamir, C.S., Rilkis, I., and Ben-David, H., (2006). Congenital Toxoplasmosis—Prenatal Aspects of Toxoplasma Gondii Infection.Reproductive toxicology, 21(4):458-472.
  • 27. Russo, S.J. and Nestler, E.J., (2013). The Brain Reward Circuitry in Mood Disorders. Nature reviews. Neuroscience 14(9).
  • 28. Vyas, A., Kim, S.K., Giacomini, N., Boothroyd, J.C., and Sapolsky, R.M., (2007). Behavioral Changes Induced by Toxoplasma Infection of Rodents are Highly Specific to Aversion of Cat Odors.Proceedings of the National Academy of Sciences 104(15): 6442-6447.
  • 29. Wang, H.L., Xiang, Y.T., Li, Q.Y., Wang, X.P., Liu, Z.C., Hao,S.S., Liu, X., Liu, L.L., Wang, G.H., and Wang, D.G., (2014). The Effect of Artemether on Psychotic Symptoms and Cognitive Impairment In First-Episode, Antipsychotic Drug-Naive Persons with Schizophrenia Seropositive to Toxoplasma Gondii.Journal of psychiatric research 53: 119-124.
  • 30. Wang, J., Li, Z., Feng, M., Ren, K., Shen, G., Zhao, C., Jin, X., and Jiang K., (2013). Opening of Astrocytic Mitochondrial ATP-Sensitive Potassium Channels Upregulates Electrical Coupling Between Hippocampal Astrocytes in Rat Brain Slices. PloS one 8(2):56605.
  • 31. Wigman, J.T., de Vos, S., Wichers, M., van Os, J., Bartels Velthuis, A.A., (2016). A Transdiagnostic Network Approach to Psychosis.Schizophrenia bulletin 43(1):122-132.
  • 32. Xiao, J., Kannan, G., Jones-Brando, L., Brannock, C., Krasnova, I., Cadet, J., Pletnikov, M., and Yolken, R., (2012). Sex-Specific Changes in Gene Expression and Behavior Induced by Chronic Toxoplasma Infection in Mice. Neuroscience 206: 39-48.
  • 33. Xu, X., Zhao, M., Liu, X., Jiang, Y., Zhang, H., Zhai, X., Zhang, L., and Hu, X., (2013). Toxoplasma Gondii Infection Regulates the Balance of Activating and Inhibitory Receptors on Decidual Natural Killer Cells.PLoS One 8(2):55432.
  • 34. Yolken, R., Dickerson, F., and Fuller Torrey, E., (2009). Toxoplasma and Schizophrenia. Parasite immunology 31(11):706-715.
  • 35. Zubor, P., Kajo, K., Dokus, K., Krivus, S., Straka, L., Bodova, K.B., and Danko, J., (2014). Recurrent Secondary Postpartum Hemorrhages Due to Placental Site Vessel Subinvolution and Local Uterine Tissue Coagulopathy.BMC Pregnancy Childbirth 14:80.

THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS

Year 2019, Volume: 14 Issue: 1, 33 - 45, 31.01.2019

Abstract

Toxoplasma Gondii is a zoonotic parasite showing intracellular localization. Although it doesn’t select a specific region in the brain tissue, the cyst forms occurring in the chronic phase may cause behavioral changes when it is located in the brain regions related to behavior. The aim of this study is to investigate whether there is a relationship between neurodegenerative and neuropsychiatric diseases caused by antibodies transmitted to the first generation of T.Gondii infection by behavioral tests. In this study, using a total of 24 female and 6 male rats. Behavioral tests have been applied to F1 generation groups female and male. In this study, female rats with chronic T.Gondii infection have been found to have increased anxiety in open field in the first generation male offsprings and decreased locomotor activity. Increased mobility in male offsprings has been observed in the elevated plus maze test. In female offspring, it has reduced anxiety and depression

References

  • 1. Arling, T.A., Yolken, R.H., Lapidus, M., Langenberg, P., Dickerson, F.B., Zimmerman, S.A., Balis, T., Cabassa, J.A., Scrandis, D.A., and Tonelli, L.H., (2009). Toxoplasma Gondii Antibody Titers and History of Suicide Attempts in Patients with Recurrent Mood Disorders. The Journal of nervous and mental disease 3(12):905-908.
  • 2. Brown, R.G., Landau, S., Hindle, J.V., Playfer, J., Samuel, M., Wilson, K.C., Hurt, C.S., Anderson, R.J., Carnell, J., and Dickinson, L., (2011). Depression and Anxiety Related Subtypes in Parkinson's Disease. Journal of Neurology, Neurosurgery & Psychiatry: jnnp. 2010.213652.
  • 3. Buentello, E., (1958). Preliminar Observations on the Relationship between Toxoplasmosis, Lysergic Acid and Schizophrenia.Gaceta medica de Mexico 88(10): 693-708.
  • 4. Caiaffa, W.T., Chiari, C.A., Figueiredo, A.R., Orefice, F., and Antunes, C.M., (1993). Toxoplasmosis and Mental Retardation: Report of a Case-Control Study. Memórias do Instituto Oswaldo Cruz 88(2): 253-261.
  • 5. Chorlton, S.D., (2017). Toxoplasma Gondii and Schizophrenia: a Review of Published RCTs. Parasitology Research: 1-7.
  • 6. Dodson, R.B., Rozance, P.J., Fleenor, B.S., Petrash, C.C., Shoemaker, L.G., Hunter, K.S., and Ferguson, V.L., (2013). Increased Arterial Stiffness and Extracellular Matrix Reorganization in Intrauterine Growth-Restricted Fetal Sheep. Pediatr Res 73(2):147-154.
  • 7. Dubey, J. and Jones, J., (2008). Toxoplasma Gondii Infection in Humans and Animals in The United States. International journal for parasitology 38(11): 1257-1278.
  • 8. Duryea, E., Nicholson, F., Cooper, S., Roberts, S., Rogers, V., McIntire, D., Sheffield, J., and Stewart R., (2015). The Use of Protease Inhibitors in Pregnancy: Maternal and Fetal Considerations. Infect Dis Obstet Gynecol 2015: 563727.
  • 9. Flegr, J., (2013). How and Why Toxoplasma Makes us Crazy. Trends in parasitology 29(4): 156-163.
  • 10. Flegr, J., Lenochová, P., Hodný, Z., and Vondrová, M., (2011). Fatal Attraction Phenomenon in Humans–Cat Odour Attractiveness Increased for Toxoplasma-Infected Men While Decreased for Infected Women. PLoS neglected tropical diseases 5(11): e1389.
  • 11. Guimarães, R.A., Asth, L., Engelberth, R. C., Souza de, J., Cavalcante, de Paula Soares-Rachetti, V., and Gavioli, E.C., (2015). Spontaneous Failure of the Estrous Eycle Induces Anxiogenic-Related Behaviors in Middle-Aged Female Mice. Physiology & behavior 147: 319-323.
  • 12. Harker, K., Ueno, N., and Lodoen, M., (2015).Toxoplasma Gondii Dissemination: a Parasite's Journey Through the Infected Host. Parasite immunology 37(3): 141-149.
  • 13. Jiao, F., Zhang, D., Jiang, M., Mi,J., Liu, X., Zhang, H., Hu, Z., Xu, X., and Hu, X., (2017). Label-Free Proteomic Analysis of Placental Proteins During Toxoplasma Gondii Infection.Journal of proteomics 150: 31-39.
  • 14. Kaur, A., Jindal, S., Kaur, I., and Chopra, K., (2013). Effect of Sesamol on the Pathophysiological Changes Induced by Surgical Menopause in Rodents.Climacteric 16(4):426-437.
  • 15. Khan, A., Dubey, J., Su, C., Ajioka, J.W., Rosenthal, B.M., and Sibley, L.D., (2011). Genetic Analyses of a Typical Toxoplasma Gondii Strains Reveal a Fourth Clonal Lineage in North America. International journal for parasitology 41(6): 645-655.
  • 16. Kusbeci, O.Y., Miman, O., Yaman, M., Aktepe, O.C., and Yazar, S., (2011). Could Toxoplasma Gondii Have Any Role in Alzheimer Disease? Alzheimer Disease & Associated Disorders 25(1):1-3.
  • 17. Liu, X., Zhao, M., Yang, X., Han, M., Xu, X., Jiang Y., and Hu,X., (2014). Toxoplasma Gondii Infection of Decidual CD1C+ Dendritic Cells Enhances Cytotoxicity of Decidual Natural Killer Cells. Inflammation 37(4):1261-1270.
  • 18. Liu, Y., Zhao, M., Xu, X., Liu, X., Zhang, H., Jiang, Y., Zhang, L., and Hu, X., (2014). Adoptive Transfer of Treg Cells Counters Adverse Effects of Toxoplasma Gondii Infection on Pregnancy.The Journal of infectious diseases, 210(9):1435-1443.
  • 19. Miman, O., Kusbeci, O.Y., Aktepe, O.C., and Cetinkaya, Z., (2010). The Probable Relation between Toxoplasma Gondii and Parkinson's Disease. Neuroscience letters 475(3):129-131.
  • 20. Misslin, R., (2003). The Defense System of Fear: Behavior and Neurocircuitry. Neurophysiologie Clinique/Clinical Neurophysiology, 33(2):55-66.
  • 21. Montoya, J.G. and Liesenfeld, O., (2004). Toxoplasmosis. Lancet 363(9425):1965-1976.
  • 22. Notarangelo, F., Wilson, E., Horning, K., Thomas, M., Harris, T., Fang, Q., Hunter, C., and Schwarcz, R., (2014). Evaluation of Kynurenine Pathway Metabolism in Toxoplasma Gondii-Infected Mice: Implications for Schizophrenia. Schizophrenia Research 152(1):261-267.
  • 23. Novotná, M., Havlíček,J., Smith, A. P., Kolbeková, P., Skallová, A., Klose, J., Gašová, Z., Písačka, M., Sechovská M., and Flegr, J. (2008). Toxoplasma and Reaction Time: Role of Toxoplasmosis in the Origin, Preservation and Geographical Distribution of Rh Blood Group Polymorphism.Parasitology, 135(11):1253-1261.
  • 24. Prandota, J., (2011). Metabolic, İmmune, Epigenetic, Endocrine and Phenotypic Abnormalities Found in Individuals With Autism Spectrum Disorders, Down Syndrome and Alzheimer Disease May be Caused by Congenital and/or Acquired Chronic Cerebral Toxoplasmosis.Research in Autism Spectrum Disorders 5(1):14-59.
  • 25. Ribeiro, D., Pereira, P., Machado, J., Silva, S., Pessoa, A., and Salvadori, D.M.F., (2004). Does Toxoplasmosis Cause DNA Damage? An Evaluation in Isogenic Mice under Normal Diet or Dietary Restriction. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 559(1):169-176.
  • 26. Rorman, E., Zamir, C.S., Rilkis, I., and Ben-David, H., (2006). Congenital Toxoplasmosis—Prenatal Aspects of Toxoplasma Gondii Infection.Reproductive toxicology, 21(4):458-472.
  • 27. Russo, S.J. and Nestler, E.J., (2013). The Brain Reward Circuitry in Mood Disorders. Nature reviews. Neuroscience 14(9).
  • 28. Vyas, A., Kim, S.K., Giacomini, N., Boothroyd, J.C., and Sapolsky, R.M., (2007). Behavioral Changes Induced by Toxoplasma Infection of Rodents are Highly Specific to Aversion of Cat Odors.Proceedings of the National Academy of Sciences 104(15): 6442-6447.
  • 29. Wang, H.L., Xiang, Y.T., Li, Q.Y., Wang, X.P., Liu, Z.C., Hao,S.S., Liu, X., Liu, L.L., Wang, G.H., and Wang, D.G., (2014). The Effect of Artemether on Psychotic Symptoms and Cognitive Impairment In First-Episode, Antipsychotic Drug-Naive Persons with Schizophrenia Seropositive to Toxoplasma Gondii.Journal of psychiatric research 53: 119-124.
  • 30. Wang, J., Li, Z., Feng, M., Ren, K., Shen, G., Zhao, C., Jin, X., and Jiang K., (2013). Opening of Astrocytic Mitochondrial ATP-Sensitive Potassium Channels Upregulates Electrical Coupling Between Hippocampal Astrocytes in Rat Brain Slices. PloS one 8(2):56605.
  • 31. Wigman, J.T., de Vos, S., Wichers, M., van Os, J., Bartels Velthuis, A.A., (2016). A Transdiagnostic Network Approach to Psychosis.Schizophrenia bulletin 43(1):122-132.
  • 32. Xiao, J., Kannan, G., Jones-Brando, L., Brannock, C., Krasnova, I., Cadet, J., Pletnikov, M., and Yolken, R., (2012). Sex-Specific Changes in Gene Expression and Behavior Induced by Chronic Toxoplasma Infection in Mice. Neuroscience 206: 39-48.
  • 33. Xu, X., Zhao, M., Liu, X., Jiang, Y., Zhang, H., Zhai, X., Zhang, L., and Hu, X., (2013). Toxoplasma Gondii Infection Regulates the Balance of Activating and Inhibitory Receptors on Decidual Natural Killer Cells.PLoS One 8(2):55432.
  • 34. Yolken, R., Dickerson, F., and Fuller Torrey, E., (2009). Toxoplasma and Schizophrenia. Parasite immunology 31(11):706-715.
  • 35. Zubor, P., Kajo, K., Dokus, K., Krivus, S., Straka, L., Bodova, K.B., and Danko, J., (2014). Recurrent Secondary Postpartum Hemorrhages Due to Placental Site Vessel Subinvolution and Local Uterine Tissue Coagulopathy.BMC Pregnancy Childbirth 14:80.
There are 35 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Articles
Authors

Erol Ayaz 0000-0001-8741-5548

Hayriye Orallar This is me 0000-0002-0000-3768

Kerem Yaman This is me 0000-0002-7009-1791

Ayhan Çetinkaya 0000-0002-8212-7149

Bihter Gökçe Bozat This is me 0000-0002-6793-6888

Mücahit Çakmak This is me 0000-0003-0361-2566

Enes Eğilmez This is me 0000-0002-2181-4025

Publication Date January 31, 2019
Published in Issue Year 2019 Volume: 14 Issue: 1

Cite

APA Ayaz, E., Orallar, H., Yaman, K., Çetinkaya, A., et al. (2019). THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS. Medical Sciences, 14(1), 33-45.
AMA Ayaz E, Orallar H, Yaman K, Çetinkaya A, Bozat BG, Çakmak M, Eğilmez E. THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS. Medical Sciences. January 2019;14(1):33-45.
Chicago Ayaz, Erol, Hayriye Orallar, Kerem Yaman, Ayhan Çetinkaya, Bihter Gökçe Bozat, Mücahit Çakmak, and Enes Eğilmez. “THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS”. Medical Sciences 14, no. 1 (January 2019): 33-45.
EndNote Ayaz E, Orallar H, Yaman K, Çetinkaya A, Bozat BG, Çakmak M, Eğilmez E (January 1, 2019) THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS. Medical Sciences 14 1 33–45.
IEEE E. Ayaz, H. Orallar, K. Yaman, A. Çetinkaya, B. G. Bozat, M. Çakmak, and E. Eğilmez, “THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS”, Medical Sciences, vol. 14, no. 1, pp. 33–45, 2019.
ISNAD Ayaz, Erol et al. “THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS”. Medical Sciences 14/1 (January 2019), 33-45.
JAMA Ayaz E, Orallar H, Yaman K, Çetinkaya A, Bozat BG, Çakmak M, Eğilmez E. THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS. Medical Sciences. 2019;14:33–45.
MLA Ayaz, Erol et al. “THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS”. Medical Sciences, vol. 14, no. 1, 2019, pp. 33-45.
Vancouver Ayaz E, Orallar H, Yaman K, Çetinkaya A, Bozat BG, Çakmak M, Eğilmez E. THE EFFECTS OF TOXOPLASMA GONDII INFECTIONS ON ANXIETY, DEPRESSION AND LEARNING IN OFFSPRINGS OF INFECTED PARENTS. Medical Sciences. 2019;14(1):33-45.