Comparison of Toxoplasma gondii IgG Antibody Levels in Children and Adolescents with Obsessive-Compulsive disorder and Attention-Deficit hyperactivity Disorder with Healthy Controls: A Cross-Sectional Study
Year 2024,
, 87 - 95, 18.03.2024
Rukiye Çolak Sivri
,
Filiz Kaya
,
Zeynep Göker
,
Ayşe Nihal Eraslan
,
Rezzan Aydın Görücü
,
Arzu Yılmaz
Abstract
Objective: This study was aimed to examine if there is a relation between IgG levels of T. gondi and OCD or ADHD symptoms.
Method: Of 42 children with OCD, 31 with ADHD and 28 healthy control were included. Children’s Yale-Brown Obsessive-Compulsive Scale (CY-BOCS), Moudsley Obession-Compulsion Inventory (MOCI), Child Depression Inventory (CDI), and Screen of Children for anxiety related disorders (SCARED), The Turgay DSM-IV-Based Child and Adolescent Behavioral Disorders Screening and Rating Scale (T-DSM-IV-S) and The Conners’ Parent Rating Scale-48 (CPRS-48) were applied. Toxo gondii IgG values ≥3.0 IU/mL were considered to be reactive. SPSS 17.0 was used for analysis. p<.05 was accepted as significant.
Results: The mean age was 12.1 years. Of 56.4% (n = 57) were boys. Depression and anxiety symptoms were similar in OCD and controls, but were significantly lower in ADHD. All children with OCD had negative (100%) for IgG levels of T. gondii, whereas 78.6% of controls and 90.3% of children with ADHD had negative for IgG levels of T. gondii. Toxo IgG seropositivity of the control was significantly higher than that of the OCD.
Toxo IgG levels were positively correlated with Turgay’s ADHD-Conduct disorder subscale scores in ADHD group (r=.650, p<.001). In the OCD and the control groups, there was no correlation between IgG levels and CDI, SCARED, ADHD scales (for all variables, p>.05).
Conclusion: To conclude, this study did not verify a relationship between the seropositivity of T. gondii with OCD and ADHD. Further studies are needed longitudinal follow-up and extended series of patients.
Supporting Institution
none
References
- Flegr J, Prandota J, Sovickova M, Israili ZH. Toxoplasmosis – A global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE 2014; 9: e90203.
- Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Sharif M, Amouei A, Daryani A. Relationship between toxoplasmosis and autism: A systematic review and meta-analysis. Microb Pathog 2020; 147: 104434.
- Rantala MJ, Luoto S, Borraz-Leon JI, Krams I. Schizophrenia: The new etiological synthesis. Neurosci Biobeh Rev 2022; 142: 104894.
- Fuglewicz AJ, Piotrowski P, Stodolak A. Relationship between toxoplasmasis and schizophrenia: A review. Adv Clin Exp Med 2017;26: 1031–6.
- Sutterland AL, Fond G, Kuin A, Koeter MW, Lutter R, van Gool T, et al. Beyond the association. Toxoplasma gondii in schizophrenia, bipolar disorder, and addiction: systematic review and meta-analysis. Acta Psychiatr Scand 2015;132:161–79.
- Krebs G, Heyman I. Obsessive–compulsive disorder in children and adolescents. Arch Dis Child 2015;100: 495–9.
- Mahjani B, Bey K, Boberg J, Burton C. Genetics of obsessive-compulsive disorder. Psychol Med 2021;51:2247–59.
- Wilbur C, Bitnun A, Kronenberg S, Laxer RM, Levy DM, Logan WJ, Shouldice M, Yeh EA. PANDAS/PANS in childhood: Controversies and evidence. Paeditr Child Health 2019;24:85–91.
- Kazemi F, Sayyah M, Tavalla M, Arjmand R. Toxoplasmosis in treatment-resistant obsessive-compulsive disorder patients. Acta Parasitol 2022;67:356-61.
- Westenberg HGM, Fineberg NA, Denys D. Neurobiology of obsessive-compulsive disorder: serotonin and beyond. CNS Spectr 2007;12:14–27.
- Drechsler R, Brem S, Brandeis D, Grünblatt E, Berger G, Walitza S. ADHD: Current concepts and treatments in children and adolescents. Neuropediatrics 2020;51:315–35.
- Kian N, Samieefar N, Rezaei N. Prenatal risk factors and genetic causes of ADHD in children. World J Pediatr 2022;18:308–19.
- Latimer K, Wilson P, Kemp J, Thompson L, Sim F, Gillberg C, Puckering C, Minnis H. Disruptive behaviour disorders: a systematic review of environmental antenatal and early years risk factors. Child Care Health Dev 2012; 38: 611-28.
- Bekdas M, Tufan AE, Hakyemez IN, Tas T, Altunhan H, Demircioglu F, Kısmet E. Subclinical immune reactions to viral infections may correlate with child and adolescent diagnosis of attention-deficit/hyperactivity disorder: a preliminary study from Turkey. Afr Health Sci 2014; 14: 439–45.
- Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA. A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE 2009; 4: e480.
- Khademvatan S, Riahi F, Izadi-Mazidi M, Khajeddin N, Yousefi E. The pediatric infectious disease journal publish ahead of print toxoplasma gondii exposure and the risk of attention deficit hyperactivity disorder in children and adolescents. Ped Infect Dis J 2018; 37: 1097–100.
- Afsharpaiman S, Khosravi MH, Faridchehr M, Komijani M. Assessment of toxoplasma seropositivity in children suffering from attention deficit hyperactivity disorder. Galen Med J 2016; 5:188–93.
- Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Amouei A, Daryani A. Toxoplasma gondii infection and risk of attention-deficit hyperactivity disorder: A systematic review and meta-analysis. Pathog Glob Health 2020;114:117–26.
- Akaltun İ, Kara T, Ayaydın H, Alyanak B, Beka H, Ağaçfidan A. The relation between serum toxoplasma gondii IgG antibody in children and ADHD and its severity. Psychiatry Clin Psychopharmacol 2019;29:326–31.
- Brem S, Grünblatt E, Drechsler R, Riederer P, Walitza S. The neurobiological link between OCD and ADHD. Atten Defic Hyperact Disord 2014;6:175–202.
- Novara C, Pardini S, Cardona F, Pastore M. Comparing models of the Children’s Yale Brown Obsessive-Compulsive Scale (CY-BOCS) in an Italian clinical sample. Front Psychiatry 2020;11:625.
- Erol N, Savaşır I. Turkish version of Maudsley Obsessive Compulsive Questionnaire. In: XXIVth National Congress of Psychiatry and Neurological Sciences, 19-23 September 1988 Ankara, Turkey, GATA Press. Congress Proceedings pages: 107–14.
- Oy B. Reliability and validity of the child depression scale. Turk Psikiyatri Derg 1991; 1: 132–6
- Çakmakçı FK. Çocuklarda anksiyete bozukluklarını tarama ölçeği geçerlik ve güvenirlik çalışması. Yayınlanmamış Uzmanlık Tezi, Kocaeli, Kocaeli Üniversitesi Tıp Fakültesi 2004.
- Turgay A. Disruptive behavior disorders child and adolescent screening and rating scales for children, adolescents, parents and teachers. West Bloomfield (Michigan): Integrative Therapy Institute Publication, 1994.
- Dereboy C, Senol S, Sener S, Dereboy F. Validation of the Turkish versions of the short-form Conners’ teacher and parent rating scales. Turk Psikiyatri Derg 2007;18: 48–58.
- Cocuzza S, Maniaci A, La Manita I, Nocera F, Caruso D, Caruso S, et al. obsessive-compulsive disorder in PANDAS/PNAS in children: In search of qualified treatment – a systematic review and metanalysis. Children (Basel) 2022; 9: 155.
- Marazziti D, Palerme S, Arone M, Massa L, Parra E, Simoncini M, et al. Obsessive-compulsive disorder, PANDAS, and Tourette syndrome: Immuno-inflammatory disorders. Adv Exp Med Biol 2023;1411:275–300.
- Thienemann M, Murphy T, Leckman J, Shaw R, Williams K, Kapphahn C, et al. clinical management of pediatric acute-onset psychiatric syndrome: Part I – Psychiatric and behavioral interventions. J Child Adolesc Psychopharmacology 2017;27: 566 –73.
- De Barros JLVM, Barbosa IG, Salem H, Rocha NP, Kummer A, Okusaga OO, et al. Is there any association between Toxoplasma gondii infection and bipolar disorder? A systematic review and meta-analysis. J Affect Disord 2017;209:59–65.
- Hajimohammadi B, Ahmadian S, Firoozi Z, Askari M, Mohammadi M, Eslami G, et al. A meta-analysis of the prevalance of toxoplasmosis in livestock and poultry worldwide. Ecohealth 2022; 19: 55–74.
- Ngoungou EB, Bhalla D, Nzoghe A, Darde ´ M-L, Preux P-M. Toxoplasmosis and epilepsy – Systematic review and meta analysis. PLoS Negl Trop Dis 2015;9: e0003525.
- Wang X, Zhang L, Lei Y, Liu X, Zhou X, Liu Y, et al. Meta-analysis of infectious agents and depression. Sci Rep 2014;4:4530.
- Brynska A, Tomaszewicz-Libudzic E, Wolanczyk T. obsessive compulsive disorder and acquired toxoplasmosis in two children. Eur Child Adolesc Psychiatry 2001;10: 200-4.
- Smadja D, Cabre P, Prat C, Vernant J. Loss of psychic auto-activation. Obsessive-compulsive behavior. Toxoplasmic abscess of the basal ganglia. Rev Neurol 1995; 151: 271-3.
- Miman O, Mutlu EA, Ozcan O, Atambay M, Karlidag R, Unal S. Is there any role of Toxoplasma gondii in the etiology of obsessive-compulsive disorder? Psychiatry Res 2010; 177: 263–5.
- Kaltuna I, Karab SS, Kara T. The relationship between Toxoplasma gondii IgG antibodies and generalized anxiety disorder and obsessive-compulsive disorder in children and adolescents: a new approach. Nordic J Psychiatry 2018;1:57–62.
- Memik NC, Tamer GS, Unver H, Gundogdu OY. The relationship between pediatric obsessive compulsive disorder and Toxoplasma gondii. J Obsessive Compuls Relat Disord 2015;7:24 -8.
- Flegr J, Hora´ček J. Toxoplasma-infected subjects report an obsessive compulsive disorder diagnosis more often and score higher in obsessive-compulsive inventory. Eur Psychiatry 2017;40: 82–7.
- Coccaro EF, Lee R, Groer MW, Can A, Coussons-Read M, Postolache TT. Toxoplasma gondii infection: relationship with aggression in psychiatric subjects. J Clin Psychiatry 2016;77: 334–1.
- Chegeni TN, Sarvi S, Amouei, Moosazadeh M, Hosseininejad Z, Aghayan SA, Daryani A. Relationship between toxoplasmosis and obsessive compulsive disorder: A systematic review and meta-analysis. PLoS Negl Trop Dis 2019;13: e0007306.
- Shehataa AI, Hassanein FI, Abdul-Ghani R. Seroprevalence of toxoplasma gondii infection among patients with non-schizophrenic neurodevelopmental disorders in Alexandria, Egypt. Acta Trop 2016; 154:155-9.
- Miman O, Ozcan O, Unal S, Atambay M. Toxoplasma gondii- obsessive compulsive disorder relationship: is it different in children? Nord J Psychiatry 2018;72: 501-5.
Obsesif kompulsif bozukluk ve Dikkat eksikliği hiperaktivite bozukluğu Olan Çocuk ve Ergenlerde Toxoplasma Gondii IgG Antikor Düzeylerinin Sağlıklı Kontrollerle Karşılaştırılması: Kesitsel Bir Çalışma
Year 2024,
, 87 - 95, 18.03.2024
Rukiye Çolak Sivri
,
Filiz Kaya
,
Zeynep Göker
,
Ayşe Nihal Eraslan
,
Rezzan Aydın Görücü
,
Arzu Yılmaz
Abstract
Amaç: Bu çalışma, T. gondi'nin IgG düzeyleri ile OKB veya DEHB belirtileri arasında bir ilişki olup olmadığını incelemek amacıyla yapılmıştır.
Yöntem: OKB'si olan 42 çocuktan 31'i DEHB'si olan ve 28 sağlıklı kontrol dahil edildi. Çocuklar için Yale-Brown Obsesif-Kompulsif Ölçeği (YB-OKB), Moudsley Obsesyon-Kompulsiyon Envanteri (MOCI), Çocuk Depresyon Ölçeği (CDI) ve Çocuklarda Anksiyete İlişkili Bozuklukları Tarama Ölçeği (ÇATÖ), Turgay DSM-IV Tabanlı Çocuk Ergen Davranış Bozuklukları Tarama ve Derecelendirme Ölçeği (T-DSM-IV-S) ve Conners Ebeveyn Değerlendirme Ölçeği-48 (CPRS-48) uygulandı. Toxo gondii IgG değerleri ≥3,0 IU/mL reaktif kabul edildi. Analiz için SPSS 17.0 kullanıldı. p<.05 anlamlı kabul edildi.
Bulgular: Ortalama yaş 12.1 yıl ve olguların %56,4'ü (n = 57) erkekti. Depresyon ve anksiyete belirtileri OKB ve kontrollerde benzerdi, ancak DEHB'de anlamlı derecede düşüktü. OKB'si olan tüm çocukların T. gondii'nin IgG seviyeleri negatifken (%100), kontrollerin %78,6'sı ve DEHB'si olan çocukların %90,3'ü T. gondii'nin IgG seviyeleri için negatifti. Kontrolün Toxo IgG seropozitifliği, OKB'ninkinden anlamlı derecede yüksekti. DEHB grubunda Toxo IgG düzeyleri ile Turgay DEHB-Davranış Bozukluğu alt ölçek puanları arasında pozitif korelasyon bulundu (r=.650, p<.001). OKB ve kontrol gruplarında IgG düzeyleri ile CDI, SCARED, DEHB ölçekleri arasında korelasyon saptanmadı (tüm değişkenler için p>.05).
Sonuç: Bu çalışma T. gondii'nin seropozitifliği ile OKB ve DEHB arasındaki ilişkiyi doğrulamamıştır. Uzunlamasına takip ve genişletilmiş hasta serileri ile daha ileri çalışmalara ihtiyaç vardır.
References
- Flegr J, Prandota J, Sovickova M, Israili ZH. Toxoplasmosis – A global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE 2014; 9: e90203.
- Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Sharif M, Amouei A, Daryani A. Relationship between toxoplasmosis and autism: A systematic review and meta-analysis. Microb Pathog 2020; 147: 104434.
- Rantala MJ, Luoto S, Borraz-Leon JI, Krams I. Schizophrenia: The new etiological synthesis. Neurosci Biobeh Rev 2022; 142: 104894.
- Fuglewicz AJ, Piotrowski P, Stodolak A. Relationship between toxoplasmasis and schizophrenia: A review. Adv Clin Exp Med 2017;26: 1031–6.
- Sutterland AL, Fond G, Kuin A, Koeter MW, Lutter R, van Gool T, et al. Beyond the association. Toxoplasma gondii in schizophrenia, bipolar disorder, and addiction: systematic review and meta-analysis. Acta Psychiatr Scand 2015;132:161–79.
- Krebs G, Heyman I. Obsessive–compulsive disorder in children and adolescents. Arch Dis Child 2015;100: 495–9.
- Mahjani B, Bey K, Boberg J, Burton C. Genetics of obsessive-compulsive disorder. Psychol Med 2021;51:2247–59.
- Wilbur C, Bitnun A, Kronenberg S, Laxer RM, Levy DM, Logan WJ, Shouldice M, Yeh EA. PANDAS/PANS in childhood: Controversies and evidence. Paeditr Child Health 2019;24:85–91.
- Kazemi F, Sayyah M, Tavalla M, Arjmand R. Toxoplasmosis in treatment-resistant obsessive-compulsive disorder patients. Acta Parasitol 2022;67:356-61.
- Westenberg HGM, Fineberg NA, Denys D. Neurobiology of obsessive-compulsive disorder: serotonin and beyond. CNS Spectr 2007;12:14–27.
- Drechsler R, Brem S, Brandeis D, Grünblatt E, Berger G, Walitza S. ADHD: Current concepts and treatments in children and adolescents. Neuropediatrics 2020;51:315–35.
- Kian N, Samieefar N, Rezaei N. Prenatal risk factors and genetic causes of ADHD in children. World J Pediatr 2022;18:308–19.
- Latimer K, Wilson P, Kemp J, Thompson L, Sim F, Gillberg C, Puckering C, Minnis H. Disruptive behaviour disorders: a systematic review of environmental antenatal and early years risk factors. Child Care Health Dev 2012; 38: 611-28.
- Bekdas M, Tufan AE, Hakyemez IN, Tas T, Altunhan H, Demircioglu F, Kısmet E. Subclinical immune reactions to viral infections may correlate with child and adolescent diagnosis of attention-deficit/hyperactivity disorder: a preliminary study from Turkey. Afr Health Sci 2014; 14: 439–45.
- Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA. A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE 2009; 4: e480.
- Khademvatan S, Riahi F, Izadi-Mazidi M, Khajeddin N, Yousefi E. The pediatric infectious disease journal publish ahead of print toxoplasma gondii exposure and the risk of attention deficit hyperactivity disorder in children and adolescents. Ped Infect Dis J 2018; 37: 1097–100.
- Afsharpaiman S, Khosravi MH, Faridchehr M, Komijani M. Assessment of toxoplasma seropositivity in children suffering from attention deficit hyperactivity disorder. Galen Med J 2016; 5:188–93.
- Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Amouei A, Daryani A. Toxoplasma gondii infection and risk of attention-deficit hyperactivity disorder: A systematic review and meta-analysis. Pathog Glob Health 2020;114:117–26.
- Akaltun İ, Kara T, Ayaydın H, Alyanak B, Beka H, Ağaçfidan A. The relation between serum toxoplasma gondii IgG antibody in children and ADHD and its severity. Psychiatry Clin Psychopharmacol 2019;29:326–31.
- Brem S, Grünblatt E, Drechsler R, Riederer P, Walitza S. The neurobiological link between OCD and ADHD. Atten Defic Hyperact Disord 2014;6:175–202.
- Novara C, Pardini S, Cardona F, Pastore M. Comparing models of the Children’s Yale Brown Obsessive-Compulsive Scale (CY-BOCS) in an Italian clinical sample. Front Psychiatry 2020;11:625.
- Erol N, Savaşır I. Turkish version of Maudsley Obsessive Compulsive Questionnaire. In: XXIVth National Congress of Psychiatry and Neurological Sciences, 19-23 September 1988 Ankara, Turkey, GATA Press. Congress Proceedings pages: 107–14.
- Oy B. Reliability and validity of the child depression scale. Turk Psikiyatri Derg 1991; 1: 132–6
- Çakmakçı FK. Çocuklarda anksiyete bozukluklarını tarama ölçeği geçerlik ve güvenirlik çalışması. Yayınlanmamış Uzmanlık Tezi, Kocaeli, Kocaeli Üniversitesi Tıp Fakültesi 2004.
- Turgay A. Disruptive behavior disorders child and adolescent screening and rating scales for children, adolescents, parents and teachers. West Bloomfield (Michigan): Integrative Therapy Institute Publication, 1994.
- Dereboy C, Senol S, Sener S, Dereboy F. Validation of the Turkish versions of the short-form Conners’ teacher and parent rating scales. Turk Psikiyatri Derg 2007;18: 48–58.
- Cocuzza S, Maniaci A, La Manita I, Nocera F, Caruso D, Caruso S, et al. obsessive-compulsive disorder in PANDAS/PNAS in children: In search of qualified treatment – a systematic review and metanalysis. Children (Basel) 2022; 9: 155.
- Marazziti D, Palerme S, Arone M, Massa L, Parra E, Simoncini M, et al. Obsessive-compulsive disorder, PANDAS, and Tourette syndrome: Immuno-inflammatory disorders. Adv Exp Med Biol 2023;1411:275–300.
- Thienemann M, Murphy T, Leckman J, Shaw R, Williams K, Kapphahn C, et al. clinical management of pediatric acute-onset psychiatric syndrome: Part I – Psychiatric and behavioral interventions. J Child Adolesc Psychopharmacology 2017;27: 566 –73.
- De Barros JLVM, Barbosa IG, Salem H, Rocha NP, Kummer A, Okusaga OO, et al. Is there any association between Toxoplasma gondii infection and bipolar disorder? A systematic review and meta-analysis. J Affect Disord 2017;209:59–65.
- Hajimohammadi B, Ahmadian S, Firoozi Z, Askari M, Mohammadi M, Eslami G, et al. A meta-analysis of the prevalance of toxoplasmosis in livestock and poultry worldwide. Ecohealth 2022; 19: 55–74.
- Ngoungou EB, Bhalla D, Nzoghe A, Darde ´ M-L, Preux P-M. Toxoplasmosis and epilepsy – Systematic review and meta analysis. PLoS Negl Trop Dis 2015;9: e0003525.
- Wang X, Zhang L, Lei Y, Liu X, Zhou X, Liu Y, et al. Meta-analysis of infectious agents and depression. Sci Rep 2014;4:4530.
- Brynska A, Tomaszewicz-Libudzic E, Wolanczyk T. obsessive compulsive disorder and acquired toxoplasmosis in two children. Eur Child Adolesc Psychiatry 2001;10: 200-4.
- Smadja D, Cabre P, Prat C, Vernant J. Loss of psychic auto-activation. Obsessive-compulsive behavior. Toxoplasmic abscess of the basal ganglia. Rev Neurol 1995; 151: 271-3.
- Miman O, Mutlu EA, Ozcan O, Atambay M, Karlidag R, Unal S. Is there any role of Toxoplasma gondii in the etiology of obsessive-compulsive disorder? Psychiatry Res 2010; 177: 263–5.
- Kaltuna I, Karab SS, Kara T. The relationship between Toxoplasma gondii IgG antibodies and generalized anxiety disorder and obsessive-compulsive disorder in children and adolescents: a new approach. Nordic J Psychiatry 2018;1:57–62.
- Memik NC, Tamer GS, Unver H, Gundogdu OY. The relationship between pediatric obsessive compulsive disorder and Toxoplasma gondii. J Obsessive Compuls Relat Disord 2015;7:24 -8.
- Flegr J, Hora´ček J. Toxoplasma-infected subjects report an obsessive compulsive disorder diagnosis more often and score higher in obsessive-compulsive inventory. Eur Psychiatry 2017;40: 82–7.
- Coccaro EF, Lee R, Groer MW, Can A, Coussons-Read M, Postolache TT. Toxoplasma gondii infection: relationship with aggression in psychiatric subjects. J Clin Psychiatry 2016;77: 334–1.
- Chegeni TN, Sarvi S, Amouei, Moosazadeh M, Hosseininejad Z, Aghayan SA, Daryani A. Relationship between toxoplasmosis and obsessive compulsive disorder: A systematic review and meta-analysis. PLoS Negl Trop Dis 2019;13: e0007306.
- Shehataa AI, Hassanein FI, Abdul-Ghani R. Seroprevalence of toxoplasma gondii infection among patients with non-schizophrenic neurodevelopmental disorders in Alexandria, Egypt. Acta Trop 2016; 154:155-9.
- Miman O, Ozcan O, Unal S, Atambay M. Toxoplasma gondii- obsessive compulsive disorder relationship: is it different in children? Nord J Psychiatry 2018;72: 501-5.