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28-10-2022 | Attention Deficit Hyperactivity Disorder | Original Article

Parasitic infections as potential risk factors for attention deficit hyperactivity disorder (ADHD) in children

Authors: Dalia A. Elmehy, Basma M. Elmansory, Ghada A. Gamea, Dina I. Abdelhai, Sherief M. Abd-Elsalam, Abeer M. Salamah, Dina S. Ata, Eman F. Mahmoud, Hoda A. Ibrahim, Amina M. Salama

Published in: Journal of Parasitic Diseases | Issue 1/2023

Abstract

Attention deficit hyperactivity disorder (ADHD) represents a mysterious neuropsychiatric alarming concern due to indefinite etiopathogenesis among children. Notably, the studies which investigated the correlation between ADHD and parasitic infections are insufficient. Therefore, this research aimed to assess the correlation between ADHD and some tissue dwelling and intestinal parasitic infections in children. The study was conducted on 200 children, including 100 children suffering from ADHD (Group I) and 100 healthy children as a control group (Group II). All caregivers fulfilled predesigned sociodemographic form and Conners parent rating scale (CPRS-48) questionnaire. Blood samples were collected to determine hemoglobin level as well as relative eosinophilic count. The presence of anti-Toxoplasma IgG and anti-Toxocara IgG in serum by Enzyme-Linked Immunosorbent Assay (ELISA) was further investigated. Also, micronutrients as zinc, iron, and copper levels were measured. Schistosoma antigen was investigated in urine samples. Stool samples were subjected to direct wet smear, concentration technique and modified Ziehl–Neelsen (MZN) staining for coccidian parasites detection. Cryptosporidium parvum, Giardia lamblia and Entamoeba histolytica antigens were investigated in stool samples. Group I expressed more liability to sociodemographic risk factors, decreased levels of Hb, iron, zinc, and copper with statistically significant difference (P < 0.001). Comparison between Group I and Group II regarding the detected parasitic infections exhibited statistically significant difference except Schistosoma antigen positivity which expressed no statistical significance. The present study concluded that the parasitic infections with their consequences are potential risk factors in children with ADHD indicating that their early diagnosis and treatment may help in ADHD prevention.

Adam I, ALhabardi NA, Al-Wutayd O, Khamis AH (2021) Prevalence of schistosomiasis and its association with anemia among pregnant women: a systematic review and meta-analysis. Parasit Vectors 14:1–10CrossRef

Ajsuvakova OP, Tinkov AA, Willkommen D, Skalnaya AA, Danilov AB, Pilipovich AA, Aschner M, Skalny AV, Michalke B, Skalnaya MG (2020) Assessment of copper, iron, zinc and manganese status and speciation in patients with Parkinson’s disease: a pilot study. J Trace Elem Med Biol 59:126423PubMedCrossRef

Allain T, Buret AG (2020) Pathogenesis and post-infectious complications in giardiasis. Adv Parasitol 107:173–199PubMedCrossRef

Bener A, Kamal M, Bener H, Bhugra D (2014) Higher prevalence of iron deficiency as strong predictor of attention deficit hyperactivity disorder in children. Ann Med Health Sci Res 4:291–297CrossRef

Blomme S, Smets L, Van Ranst M, Boeckx N, Van Laer C (2020) The influence of COVID-19 on routine hematological parameters of hospitalized patients. Acta Clin Belg. https://doi.org/10.1080/17843286.2020.1814649CrossRefPubMed

Brahem M, Hlel K, Ayadi A, Bedoui A, Hmila F, Mahjoub B, Boussoffara R, Sfar MT (2006) Cerebral hydatid cysts in children: 4 cases. Med Mal Infect 36:434–437PubMedCrossRef

Cabral CM, Tuladhar S, Dietrich HK, Nguyen E, MacDonald WR, Trivedi T, Devineni A, Koshy AA (2016) Neurons are the primary target cell for the brain-tropic intracellular parasite Toxoplasma gondii. PLoS Pathog 12:1005447CrossRef

Carter CJ (2013) Toxoplasmosis and polygenic disease susceptibility genes: extensive Toxoplasma gondii host/pathogen interactome enrichment in nine psychiatric or neurological disorders. J Pathog. 2013:1–29CrossRef

Catale C, Geurten M, Lejeune C, Meulemans T (2014) The Conners Parent Rating Scale: psychometric properties in typically developing 4-to 12-year-old Belgian French-speaking children. Eur Rev Appl Psychol 64:221–227CrossRef

Chen K, Zheng X, Li Z, Xiang H, Chen B, Zhang H (2019) Risk factors analysis of attention deficit/hyperactivity disorder and allergic rhinitis in children: a cross-sectional study. Ital J Pediatr 45:1–7CrossRef

Colley DG, King CH, Kittur N, Ramzy RM, Secor WE, Fredericks-James M, Ortu G, Clements MN, Ruberanziza E, Umulisa I, Wittmann U (2020) Evaluation, validation, and recognition of the point-of-care circulating cathodic antigen, urine-based assay for mapping Schistosoma mansoni infections. Am J Trop Med Hygiene 103(1_Suppl):42–49CrossRef

Cortese S, Angriman M, Lecendreux M, Konofal E (2012) Iron and attention deficit/hyperactivity disorder: what is the empirical evidence so far? A systematic review of the literature. Expert Rev Neurother 12:1227–1240PubMedCrossRef

Davoudi M, Rafiei Sefiddashti R, Meamar A, Toreyhi S, Hadighi R (2020) Intestinal parasites and theta brainwave changes in children. J Compr Pediatr 11(4):e103015. https://doi.org/10.5812/compreped.103015CrossRef

Demontis D, Walters RK, Rajagopal VM, Waldman ID, Grove J, Als TD, Dalsgaard S, Ribasas M, Bybjerg-Grauholm J, Bækvad-Hansen M, Werge T (2021) Risk variants and polygenic architecture of disruptive behavior disorders in the context of attention-deficit/hyperactivity disorder. Nat Commun 12:1–12

El-Beshbishi SN, El-Tantawy NL, Elzeky SM, Abdalaziz KF, Atia RA (2018) Seroprevalence of Toxoplasma gondii infection in children with central nervous system disorders in Mansoura, Egypt: a case–control study. Trans R Soc Trop Med Hyg 112:555–560PubMed

Erikson KM, Jones BC, Beard JL (2000) Iron deficiency alters dopamine transporter functioning in rat striatum. J Nutr 130:2831–2837PubMedCrossRef

Ezeamama AE, Bustinduy AL, Nkwata AK, Martinez L, Pabalan N, Boivin MJ, King CH (2018) Cognitive deficits and educational loss in children with schistosome infection—a systematic review and meta-analysis. PLoS Negl Trop Dis 12:e0005524PubMedPubMedCentralCrossRef

Geneidy MR (2019) A study on intestinal parasitic infections among immunocompetent egyptian children attending Al-Hussein University Hospital, Cairo. Egypt J Hosp Med 77:5322–5337CrossRef

Heikkilä AR, Elovainio M, Raaska H, Matomäki J, Sinkkonen J, Lapinleimu H (2021) Intestinal parasites may be associated with later behavioral problems in internationally adopted children. PLoS ONE 16(1):e0245786PubMedPubMedCentralCrossRef

Hemamy M, Heidari-Beni M, Askari G, Karahmadi M, Maracy M (2020) Effect of Vitamin D and magnesium supplementation on behavior problems in children with attention-deficit hyperactivity disorder. Int J Prevent Med 11:4CrossRef

Hermes G, Ajioka JW, Kelly KA, Mui E, Roberts F, Kasza K, Mayr T, Kirisits MJ, Wollmann R, Ferguson DJ, Roberts CW (2008) Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. J Neuroinflamm 5:1–37CrossRef

Hussein EM, Zaki WM, Ahmed SA, Almatary AM, Nemr NI, Hussein AM (2016) Predominance of Giardia lamblia assemblage A among iron deficiency anaemic pre-school Egyptian children. J Parasitol Res 115:1537–1545CrossRef

Ismail HI, Hamouda HE, Baalash AA, Haiba AA, Ismail CM, Shamloula MM (2007) Immunohistochemical and neurotransmitter changes in the brain of mice infected with hymenolepis nana. Tanta Med Sci J 2:117–132

Koszewiczz M, Jaroch J, Brzecka A, Ejma M, Budrewicz S, Mikhaleva LM, Muresanu C, Schield P, Somasundaram SG, Kirkland CE, Avila-Rodriguez M (2020) Dysbiosis is one of the risk factor for stroke and cognitive impairment and potential target for treatment. Pharmacol Res 164:105277CrossRef

Lam AP, de Sordi D, Müller HH, Lam MC, Carl A, Kohse KP, Philipsen A (2020) Aggravation of symptom severity in adult attention-deficit/hyperactivity disorder by latent Toxoplasma gondii infection: a case–control study. Sci Rep 10(1):1–16CrossRef

Lompo LD, Kamdem FK, Revenco E, Allibert R, Medeiros E, Vuillier F, Moulin T (2012) Toxocara canis cerebral vasculitis revealed by iterative strokes. Rev Neurol 168:533–537PubMedCrossRef

Lu CW, Lee YC, Kuo CS, Chiang CH, Chang HH, Huang KC (2021) Association of serum levels of zinc, copper, and iron with risk of metabolic syndrome. Nutrients 13(2):548PubMedPubMedCentralCrossRef

Mahmoud AM, Abdul Fattah M, Zaher TI, Abdel-Rahman SA, Mosaad N (2017) Intestinal parasitic infections and iron deficiency anaemia among school children in El Khalige Village, Dakhalia, Egypt. Afro-Egypt J Infect Endem Dis 7:28–36

Maiga Y, Wiertlewski S, Desal H, Marjolet M, Damier P (2007) Toxocarose cérébrale révélée par une confusion mentale chez un adulte à Nantes: cas clinique et revue de la littérature. Bulletin De La Société De Pathologie Exotique 100:101–104PubMed

Marques RC, Bernardi JV, Dorea CC, Dórea JG (2020) Intestinal parasites, anemia and nutritional status in young children from transitioning western Amazon. Int J Environ Res Public Health 17(2):577PubMedPubMedCentralCrossRef

Mnkugwe RH, Minzi OS, Kinung’hi SM, Kamuhabwa AA, Aklillu E (2020) Prevalence and correlates of intestinal schistosomiasis infection among school-aged children in North-Western Tanzania. PLoS ONE 15(2):e0228770PubMedPubMedCentralCrossRef

Nayeri T, Sarvi S, Moosazadeh M, Hosseininejad Z, Amouei A, Daryani A (2020) Toxoplasma gondii infection and risk of attention-deficit hyperactivity disorder: a systematic review and meta-analysis. Pathog Glob Health 114(3):126–135CrossRef

Nicoletti A (2020) Neurotoxocariasis. Adv Parasitol 109:219–231PubMedCrossRef

Noorazar SG, Malek A, Aghaei SM, Yasamineh N, Kalejahi P (2020) The efficacy of zinc augmentation in children with attention deficit hyperactivity disorder under treatment with methylphenidate: a randomized controlled trial. Asian J Psychiatr 48:101868PubMedCrossRef

Noori MA, AL-Hasnawi SMJ, AL-Haidari AF, Hamza DM (2020) Toxoplasma gondii seropositivity and attention deficit hyperactivity disorder. J Glob Sci Res 10:871–879

Nourredine M, Gering A, Fourneret P, Rolland B, Falissard B, Cucherat M, Geoffray MM, Jurek L (2021) Association of attention-deficit/hyperactivity disorder in childhood and adolescence with the risk of subsequent psychotic disorder: a systematic review and meta-analysis. JAMA Psychiat 78(5):519–529CrossRef

Oner O, Oner P, Bozkurt OH, Odabas E, Keser N, Karadag H, Kızılgün M (2010) Effects of zinc and ferritin levels on parent and teacher reported symptom scores in attention deficit hyperactivity disorder. Child Psychiatry Hum Dev 41(4):441–447PubMedPubMedCentralCrossRef

Oner P, Oner O, Azik FM, Cop E, Munir KM (2012) Ferritin and hyperactivity ratings in attention deficit hyperactivity disorder. Pediatr Int 54:688–692PubMedPubMedCentralCrossRef

Othman AA, Abdel-Aleem GA, Saied EM, Mayah WW, Elatrash AM (2010) Biochemical and immunopathological changes in experimental neurotoxocariasis. Mol Biochem Parasitol 172:1–8PubMedCrossRef

Robberecht H, Verlaet AA, Breynaert A, De Bruyne T, Hermans N (2020) Magnesium, iron, zinc, copper and selenium status in attention-deficit/hyperactivity disorder (ADHD). Molecules 25(19):4440PubMedPubMedCentralCrossRef

Robinson G, Chalmers RM (2020) Cryptosporidium diagnostic assays: microscopy. In: Mead J, Arrowood M (eds) Cryptosporidium. Humana, New York, NY, pp 1–10

Rodríguez C, Álvarez D, Gónzalez-Castro P, García JN, Alvarez L, Núñez JC, González JA, Bernado A (2021) ADHD and Writing learning disabilities: comorbidity in basis of attention and working memory. Eur J Educ Psychol. https://doi.org/10.30552/ejep.v2i3.34CrossRef

Samie A, Mahlaule L, Mbati P, Nozaki T, ElBakri A (2020) Prevalence and distribution of Entamoeba species in a rural community in northern South Africa. Food Waterborne Parasitol 18:e00076PubMedPubMedCentralCrossRef

Shalaby NM, Shalaby NM, Sayed AO (2017) Impact of parasitic infections on nutritional status and micronutrients in Saudi children. Curr Pediatr Res 21(1):1–7

Skallova A, Kodym P, Frynta D, Flegr J (2006) The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology 133:525–535. https://doi.org/10.1017/s0031182006000886CrossRefPubMed

Skalny AV, Mazaletskaya AL, Ajsuvakova OP, Bjørklund G, Skalnaya MG, Chao JCJ, Chernova LN, Shakieva RA, Kopylov PY, Skalny AA, Tinkov AA (2020) Serum zinc, copper, zinc-to-copper ratio, and other essential elements and minerals in children with attention deficit/hyperactivity disorder (ADHD). J Trace Elem Med Biol 58:126445PubMedCrossRef

Sucheta JL, Chandi DH, Som JL (2021) Study of parasitic infection in immunosuppressive patients and its association with the socio-demographic status. J Clin Diagn Res. https://doi.org/10.7860/JCDR/2021/47351.14424CrossRef

Teja SS, Swarna SR, Jeyakumari D, Kanna V (2020) A study on intestinal parasitic infections among school children in Karaikal. Trop Parasitol 10(2):79PubMedCrossRef

Tonelli LH, Katz M, Kovacsics CE, Gould TD, Joppy B, Hoshino A, Hoffman G, Komarow H, Postolache TT (2009) Allergic rhinitis induces anxiety-like behavior and altered social interaction in rodents. Brain Behav Immun 23:784–793PubMedPubMedCentralCrossRef

Turrin NP, Plata-Salamán CR (2000) Cytokine–cytokine interactions and the brain. Brain Res Bull 51:3–9PubMedCrossRef

Viktorinova A, Trebaticka J, Paduchova Z, Ursinyova M, Uhnakova I, Masanova V, Durackova Z (2009) WITHDRAWN: natural polyphenols modify trace element status and improve clinical symptoms of attention-deficit hyperactivity disorder. Biomed Pharmacother. https://doi.org/10.1016/j.biopha.2009.04.040CrossRefPubMed

Volkow ND, Wang GJ, Kollins SH, Wigal TL, Newcorn JH, Telang F, Fowler JS, Zhu W, Logan J, Ma Y, Pradhan K (2009) Evaluating dopamine reward pathway in ADHD: clinical implications. J Am Med Assoc 302:1084–1091CrossRef

Webster JP, Lamberton PHL, Donnelly CA, Torrey EF (2006) Parasites as causative agents of human affective disorders? The impact of anti-psychotic, mood-stabilizer and anti-parasite medication on Toxoplasma gondii’s ability to alter host behaviour. Proc R Soc B 273:1023–1030. https://doi.org/10.1098/rspb.2005.3413CrossRefPubMedPubMedCentral

Wiser MF (2021) Nutrition and protozoan pathogens of humans: a primer. In: Humphries DL, Scott ME, Vermund SH (eds) Nutrition and infectious diseases. Humana, Cham, pp 165–187CrossRef

Wood DR, Reimherr FW, Wender PH (1985) Amino acid precursors for the treatment of attention deficit disorder, residual type. Psychopharmacol Bull 21:146–149PubMed

Zhu Q, Dai Y, Zhang J, Xie W, Zuo H, Zhang J, Zhou Y (2021) Association between serum zinc concentrations and metabolic risk factors among Chinese children and adolescents. Br J Nutr. https://doi.org/10.1017/S0007114521000258CrossRefPubMedPubMedCentral

Title: Parasitic infections as potential risk factors for attention deficit hyperactivity disorder (ADHD) in children
Authors: Dalia A. Elmehy
Basma M. Elmansory
Ghada A. Gamea
Dina I. Abdelhai
Sherief M. Abd-Elsalam
Abeer M. Salamah
Dina S. Ata
Eman F. Mahmoud
Hoda A. Ibrahim
Amina M. Salama
Publication date: 28-10-2022
Publisher: Springer India
Keywords: Attention Deficit Hyperactivity Disorder
Entamoeba Histolytica
Attention Deficit Hyperactivity Disorder
Published in: Journal of Parasitic Diseases / Issue 1/2023
Print ISSN: 0971-7196
Electronic ISSN: 0975-0703
DOI: https://doi.org/10.1007/s12639-022-01542-x

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