The association between seropositivity to human toxocariasis and childhood asthma in northern Iran: a case-control study

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Sorena Darvish
Iraj Mohammadzadeh
Saeed Mehravar
Adel Spotin
Ali Rostami


Toxocara infection, association, childhood asthma, ELISA, Iran.


Background: Besides the well-known risk factors, Toxocara infection is thought to play a significant etiological role in the development of childhood asthma. To further explore this association, the prevalence of Toxocara infection in sera of asthmatic children and healthy controls in northern Iran was investigated.

Methods: In this case-control study, cases were 145 physician-confirmed asthmatic children diagnosed according to the Global Initiative for Asthma (GINA) guidelines. Controls were 115 age–sex–residence-matched children who did not have physician-diagnosed asthma. The presence of anti-Toxocara immunoglobulin G (IgG) was tested using enzyme-linked immunosorbent assay. Univariate and multivariate logistic regression methods were used for case-control comparisons.

Results: Seropositivity rate was 4.1% (95% CI, 3.4–4.7%) in asthmatic children and 0.86% (95% CI, 0.71–1.0%) in controls, suggesting a strong association (P-value < 0.02). Moreover, Toxocara infection was not significantly more prevalent (P-value = 0.12) in children with moderate sustainable asthma (9.3%, 3/32) than in children with mild sustainable asthma (2.3%, 3/113). Mean total immunoglobulin E (IgE) level was significantly higher in Toxocara-infected children (222.3 ± 367.1) than in non-infected children (143.19 ± 218.05) in the case group (P-value < 0.05).

Conclusions: Our findings indicated that Toxocara infection can play an important role in childhood asthma. Further experimental and epidemiological studies are needed to clarify this hypothesis.

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1. Fakhri Y, Gasser R, Rostami A, Fan C, Ghasemi S, Javanian M, et al. Toxocara eggs in public places worldwide – a systematic review and meta-analysis. Environ Pollut. 2018;242:1467–1475.

2. Ma G, Holland CV, Wang T, Hofmann A, Fan C-K, Maizels RM, et al. Human toxocariasis. Lancet Infect Dis. 2018;18(1): e14–e24.

3. Rostami A, Sepidarkish M, Ma G, Wang T, Ebrahimi M, Fakhri Y, et al. Global prevalence of Toxocara infection in cats. Adv Parasitol. 2020;109:615–639. bs.apar.2020.01.025

4. Rostami A, Riahi SM, Hofmann A, Ma G, Wang T, Behniafar H, et al. Global prevalence of Toxocara infection in dogs. Adv Parasitol. 2020;109:561–583. bs.apar.2020.01.017

5. Rostami A, Ma G, Wang T, Koehler AV, Hofmann A, Chang BC, et al. Human toxocariasis – a look at a neglected disease through an epidemiological ‘prism’. Infect Genet Evol. 2019:74;104002. meegid.2019.104002

6. Rostami A, Riahi SM, Fallah Omrani V, Wang T, Hofmann A, Mirzapour A, et al. Global prevalence estimates of Toxascaris leonina infection in dogs and cats. Pathogens. 2020;9(6):503.

7. Ma G, Rostami A, Wang T, Hofmann A, Hotez PJ, Gasser RB. Global and regional seroprevalence estimates for human toxo-cariasis: a call for action. Adv Parasitol. 2020;109:275–290.

8. Mohammadzadeh I, Riahi SM, Saber V, Darvish S, Amrovani M, Arefkhah N, et al. The relationship between Toxocara species seropositivity and allergic skin disorders: a system-atic review and meta-analysis. Trans R Soc Trop Med Hyg. 2018;112(12):529–537.

9. Baghani Z, Khazan H, Sohrabi MR, Rostami A. Seroprevalence of Toxocara infection among healthy individuals referred to the medical center laboratories in Tehran City, Capital of Iran. Novel Biomed. 2018;6(2):68–73. v6i2.16938

10. Fischer N, Rostaher A, Zwickl L, Deplazes P, Olivry T, Favrot C. A Toxocara canis infection influences the immune response to house dust mite allergens in dogs. Vet Immunol Immunopathol. 2018;202:11-7. vetimm.2018.06.009

11. Roth GA, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, et al. Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392(10159):1736–1788. https://doi. org/10.1016/S0140-6736(18)32203-7

12. Kyu HH, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, et al. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392(10159):1859–1922. https://doi. org/10.1016/S0140-6736(18)32335-3

13. Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16(1):45.

14. Aghaei S, Riahi SM, Rostami A, Mohammadzadeh I, Javanian M, Tohidi E, et al. Toxocara spp. infection and risk of childhood asthma: a systematic review and meta-analysis. Acta Trop. 2018;182:298–304. 2018.03.022

15. Cooper P. Toxocara canis infection: an important and neglected environmental risk factor for asthma? [This edito-rial discusses the findings of the paper in this issue by E. Pinelli et al. [19], pp 649–658.] Clin Exp Allergy. 2008;38(4):551–553.

16. Pinelli E, Brandes S, Dormans J, Gremmer E, Van Loveren H. Infection with the roundworm Toxocara canis leads to exacerbation of experimental allergic airway inflamma-tion. Clin Exp Allergy. 2008;38(4):649–658. https://doi. org/10.1111/j.1365-2222.2007.02908.x

17. Rostami A, Seyyedtabaei SJ, Aghamolaie S, Behniafar H, Lasjerdi Z, Abdolrasouli A, et al. Seroprevalence and risk fac-tors associated with Toxoplasma gondii infection among rural communities in northern Iran. Rev Inst Med Trop Sao Paulo. 2016;58:70.

18. Rostami A, Mozafari M, Gholipourmalekabadi M, Caicedo HH, Lasjerdi Z, Sameni M, et al. Optimization of fluoride-con-taining bioactive glasses as a novel scolicidal agent adjunct to hydatid surgery. Acta Trop. 2015;148:105–114. https://doi. org/10.1016/j.actatropica.2015.04.021

19. Siyadatpanah A, Tabatabaei F, Zeydi AE, Spotin A, Fallah-Omrani V, Assadi M, et al. Parasitic contamination of raw vegetables in Amol, North of Iran. Arch Clin Infect Dis. 2013;8(2):e15983.

20. Aghamolaie S, Seyyedtabaei SJ, Behniafar H, et al. Seroepidemiology, modifiable risk factors and clinical symptoms of Toxocara spp. infection in northern Iran. Trans R Soc Trop Med Hyg. 2019;113:116–122. trstmh/try118

21. Mohammadzadeh I, Ghafari J, Savadkoohi RB, Tamaddoni A, Dooki MRE, Navaei RA. The prevalence of asthma, aller-gic rhinitis and eczema in north of Iran. Iran J Pediatr. 2008;18(2):117–122.

22. Mohammadzadeh I, Rostami A, Darvish S, Mehravar S, Pournasrollah M, Javanian M, et al. Exposure to Ascaris lum-bricoides infection and risk of childhood asthma in north of Iran. Infection. 2019: 47(6):991–999. s15010-019-01343-0.

23. Becker AB, Abrams EM. Asthma guidelines: the Global Initiative for Asthma in relation to national guidelines. Curr Opin Allergy Clin Immunol. 2017;17(2):99–103. https://doi. org/10.1097/ACI.0000000000000346

24. Buijs J, Borsboom G, van Gemund JJ, et al. Toxocara sero-prevalence in 5-year-old elementary schoolchildren: relation with allergic asthma. Am J Epidemiol. 1994;140(9):839–847.

25. Buijs J, Borsboom G, van Gemund JJ, Hazebroek A, van Dongen PA, van Knapen F, et al. Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children. Eur Respir J. 199710(7): 1467–1475.

26. Cobzaru R-G, Rîpă C, Leon MM, Luca MC, Ivan A, Luca M. Correlation between asthma and Toxocara canis infection. Rev Med Chir Soc Med Nat Iasi. 2012;116(3):727–730.

27. Fernando D, Wickramasinghe P, Kapilananda G, Dewasurendra RL, Amarasooriya M, Dayaratne A. Toxocara seropositivity in Sri Lankan children with asthma. Pediatr Int. 2009;51(2):241–245.

28. Hakim SL, Thadasavanth M, Shamilah RR, Yogeswari S. Prevalence of Toxocara canis antibody among children with bronchial asthma in Klang Hospital, Malaysia. Trans R Soc Trop Med Hyg. 1997;91(5):528. S0035-9203(97)90010-9

29. Kanobana K, Vereecken K, Junco Diaz R, Sariego I, Rojas L, Bonet Gorbea M, et al. Toxocara seropositivity, atopy and asthma: a study in Cuban schoolchildren. Trop Med Int Health. 2013;18(4):403–406.

30. Muñoz-Guzmán M, del Río-Navarro BE, Valdivia-Anda G, Alba-Hurtado F. The increase in seroprevalence to Toxocara canis in asthmatic children is related to cross-reaction with Ascaris suum antigens. Allergol Immunopathol. 2010;38(3):115–121.

31. Cadore PS, Zhang L, Lemos LdL, Lorenzi C, Telmo PdL, dos Santos PC, et al. Toxocariasis and childhood asthma: a case-control study. J Asthma. 2016;53(6):601–606. https://doi. org/10.3109/02770903.2015.1064951

32. Chan PW, Anuar AK, Fong MY, Debruyne JA, Ibrahim J. Toxocara seroprevalence and childhood asthma among Malaysian children. Pediatr Int. 2001;43(4):350–353. https://

33. Figueiredo SD, Taddei JA, Menezes JJ, Novo NF, Silva EO, Cristóvão HL, et al. Clinical-epidemiological study of toxocariasis in a pediatric population. J Pediatr. 2005;81(2):126–132. https://

34. Mendonça LR, Veiga RV, Dattoli VCC, Figueiredo CA, Fiaccone R, Santos J, et al. Toxocara seropositivity, atopy and wheezing in children living in poor neighbourhoods in urban Latin American. PLoS Negl Trop Dis. 2012;6(11):e1886. https://

35. Mosayebi M, Moini L, Hajihossein R, Didehdar M, Eslamirad Z. Detection of specific antibody reactivity to Toxocara larval excretory-secretory antigens in asthmatic patients (5-15 years). Open Microbiol J. 2016;10:162. https://doi. org/10.2174/1874285801610010162

36. Sharghi N, Schantz PM, Caramico L, Ballas K, Teague BA, Hotez PJ. Environmental exposure to Toxocara as a possible risk factor for asthma: a clinic-based case-control study. Clin Infect Dis. 2001;32(7):e111–e116.https://doi. org/10.1086/319593

37. Silva MB, Amor AL, Santos LN, Galvão AA, Vera AVO, Silva ES, et al. Risk factors for Toxocara spp. seroprevalence and its association with atopy and asthma phenotypes in school-age children in a small town and semi- rural areas of Northeast Brazil. Acta Trop. 2017;174:158–164. actatropica.2016.04.005

38. Pinelli E, Withagen C, Fonville M, Verlaan A, Dormans J, Van Loveren H, et al. Persistent airway hyper-responsiveness and inflammation in Toxocara canis-infected BALB/c mice. Clin Exp Allergy. 2005;35(6):826–832. 10.1111/j.1365-2222.2005.02250.x

39. Carlos D, Sá-Nunes A, de Paula L, Matias-Peres C, Jamur MC, Oliver C, et al. Histamine modulates mast cell degranulation through an indirect mechanism in a model IgE-mediated reaction. Eur J Immunol. 2006;36(6):1494–1503. https://doi. org/10.1002/eji.200535464

40. Rostami A, Riahi S, Holland C, Taghipour A, Khalili-Fomeshi M, Fakhri Y, et al. Seroprevalence estimates for toxocariasis in people worldwide: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2019;13(12):e0007809. https://doi. org/10.1371/journal.pntd.0007809