Introduction

Toxocariasis is an infection of a human by the larvae of Toxocara canis (dog roundworm) or Toxocara cati (cat roundworm) [1]. Adult worms of Toxocara parasite live in the small intestine of dogs or cats. Exposure to an infected hosts’ feces, typically by ingestion of contaminated soil, allows transmission of Toxocara to humans. T canis is the main cause of toxocariasis, and syndromes such as ocular larva migrans, cerebral larva migrans, cutaneous larva migrans and visceral larva migrans (mainly liver and lungs) arise [2, 3].

In 1952, Beaver et al [4] reported blood eosinophilia in 3 children at a level that is associated with chronic granulomatous lesions of the liver, and for the first time T canis larvae were found in the liver, this new disease was named visceral larvemigran. Beaver came to the conclusion that humans serve as a paratenic host; larvae development is arrested. He believed that others Toxocara species could also cause visceral larva migrans in humans [4].

Epidemiology studies show that humans become infected with Toxocara by eating soil containing embryonated eggs [5] classifying toxocariasis as a soil transmitted disease. However, eating Toxocara-infected meat of a paratenic host (small animals and domestic animals) causes toxocariasis, thus the infection is a food transmissible disease too [6]. Eating raw or undercooked Toxocara-infected meat of birds and mammals causes toxocariasis [7–9].

Epidemiological studies have shown that toxocariasis is 1 of the most common helminthic diseases in the world [3, 10, 11]. The worldwide prevalence of toxocariasis has been reported as 2–5% in urban areas, 15–20% in semi-rural areas and 35–42% in rural areas [2].

Low socioeconomic status and poor living standards are contributing factors in the spread of disease [12]. Most infections have no clinical symptoms although many Toxocara larvae are released in the body and may cause dangerous side effects including; weight loss, fever with cough and shortness of breath, generalized lymphadenopathy and hepatomegaly [8, 13, 14]. Diagnosis of toxocariasis by hematology involves an eosinophil cell count and serology [15].

Despite the global spread of Toxocara, the prevalence of toxocariasis in Ilam has not been comprehensively studied in children, though highly prevalent. Ilam has a high frequency of stray dogs and cats that are definitive hosts for Toxocara, and a low level of sanitary conditions especially in rural areas. The purpose of this study was to evaluate the prevalence of Toxocara in children aged 10 years and younger, in urban and rural areas in Ilam province.

Materials and Methods

Approval for this study was granted by the Ethics Committee of Ilam, University of Medical Sciences (No. 679).

1. Demographics

This study was a cross-sectional study performed on children ≤ 10 years old from rural or urban areas of Ilam province, west Iran. This area covers 19,086 square kilometers and includes 8 cities: Ilam, Mehran, Dehloran, DarrehShahr, Sarable, Eyvan, Abdanan and Arkwaz.

Ilam province shares its borders with 3 neighboring Iranian provinces: Khuzestan province in the south, Lurestan province in the east, Kermanshah province in the north, and Iraq in the west. There are 425 km of common border. The population of Ilam province is approximately 600,000 people (2015 estimate).

2. Detection of Toxocara

383 children were randomly selected and blood samples were taken, and transferred to the laboratory of Parasitology, Ilam University of Medical Sciences for laboratory investigation. Blood samples were separated by centrifugation at 5000 rpm for 5 minutes and the serum was removed and stored at −20 °C. Detection of Toxocara antibody in the serum was performed using an enzyme-linked immunosorbent assay (ELISA) kit (IBL Hamburg in Germany). A positive result was determined by a value more than 0.5 (100 ng/mL) and a negative result was defined by a value less than 0.5.

3. Characteristics

A questionnaire was designed to capture personal characteristics, residence location, dog ownership in the family or extended family, history of eating or playing with dirt and anti-parasitic drug history.

4. Statistical analysis

The sample size was calculated using the formula Cochrane 383. Chi-square test, t test and Mann-Whitney nonparametric test were used to determine risk factors and outbreaks. The level of statistical significance was set at p < 0.05 (SPSS17 software was used for data analysis).

Results

From the total number of 383 children ≤ 10 years old that were selected for this study, 205 were males and 178 were females. There were 154 children that were from a rural environment and 229 that were from an urban environment. Only 78 children stated a history of contact with dogs and cats, and 11 children had a history of pica.

In this study the prevalence rate of toxocariasis was 23% in males, 18% in females. Rural children accounted for 36% of toxocariasis cases and urban children accounted for 20%. Overall, 22% of all children had toxocariasis; 31% in children who had dogs, and 14% in children who did not own a dog or a cat.

A significant association was found between the risk of toxocariasis and, urban life, rural life, and history of contact with dogs and cats (p < 0.05). No significant association was observed between toxocariasis and, a history of pica, gender or age.

Discussion

The results from this study can inform pediatricians and be used by health centers to educate and help reduce the risk of toxocariasis in children. When children present with a chronic cough, the medical notes may reflect a diagnosis of asthma and corticosteroid treatment, whilst parasitic infections such as Toxocara should also be noted in the incidence of these diseases.

The results of this study show that exposure to Toxocara in children 10 years and younger in Ilam is sizable; regardless of whether they are symptomatic or asymptomatic, or with or without significant eosinophilia. Toxocariasis in Ilam province can be classified as hyper-endemic.

Climate, geographical condition, owing a pet dog or cat (kept inside the home), owning a working dog (in rural area) and the presence of stray dogs and cats in public parks all contribute to the spread of Toxocara [16].

It has been reported that only 2% of urban and rural school children (6 to 15 years) in Ahvaz had IgG antibodies against Toxocara. Although, Ahvaz is part of the tropics, where favorable conditions increase the prevalence of infectious diseases, the author questioned these results suggesting that there may have been an issue with the serology tests [17]. It may be that hot and dry weather conditions caused the loss or inactivation of the Toxocara eggs.

In a study carried out in the city of Babol (northern Iran), the prevalence of infection with Toxocara in adults with eosinophilia, was 23.5%. A significant difference was reported between residence and work place with toxocariasis. In this study, the prevalence of Toxocara was significantly associated with the location [10]. In a study performed by Malla et al in northern India, 6.4% of asymptomatic rural people, and 23.3% of symptomatic rural people had anti-Toxocara antibody(18). In study by Fan et al [19], Hei-dong and Yen-ping districts in Taitung County of eastern Taiwan, showed that overall sero-prevalence of Toxocara was 76% using ELISA among students aged 7 to 12, that is higher than of the results of the present study.

The amount of contact with dogs and cats for religious reasons as well as race-dependent susceptibility to Toxocara are some theories that may explain these differences [20]. Of course, other factors such as cut-off points used for testing and the sensitivity and specificity of the serologic tests can affect the results [21]. Sajadi et al [22] conducted a study on serum samples of 516 children aged 6–13 years using ELISA and the overall prevalence of anti-Toxocara antibody was 25.6%. This result is in concordance with the results of this present study. Ajayi et al [23] reported that 30.4% of adults and 29.6% of children in Nigeria had anti-Toxocara antibodies. In studies that were conducted on symptomatic, eosinophilic people, the prevalence rate of toxocariasis was reported to be higher than in the general public and in most of the aforementioned papers there was no reporting on an association between age and gender with seroprevalence of Toxocara [12, 13, 24, 25].

Most of the reported studies of toxocariasis were conducted in children because in their early years they exhibit pica and could be exposed to Toxocara from infected dogs and cats, and asymptomatic adults. In the present study no association was found between owning dogs and prevalence of toxocariasis, however, a study conducted by Ebrahimifard et al [10], found an association between exposure to (rather than owning) dogs and cats, and toxocariasis.

In Ilam province, because of religious and social conditions, the dog is viewed as “unclean” and people do not have direct or close contact with them, but dogs and cats do roam freely.

The results of this study showed that Toxocara infection is high amongst the children of Ilam and preventive work such as risk management and treatment/elimination of stray dogs and cats is necessary. Larger studies to determine seroprevalence of infection with Toxocara in children and adults needs to be performed.

Article information

Conflicts of Interest

No potential conflicts of interest relevant to this article was reported.

References

• 1. Abdi J, Darabi M, Sayehmiri K. Epidemiological situation of toxocariasis in Iran: meta-analysis and systematic review. Pak J Biol Sci 2012;15(22): 1052−5. PMID: 10.3923/pjbs.2012.1052.1055.ArticlePubMed
• 2. Magnaval JF, Glickman LT, Dorchies P, et al. Highlights of human toxocariasis. Korean J Parasitol 2001;39(1): 1−11. PMID: 10.3347/kjp.2001.39.1.1. PMID: 11301585. PMID: 2721060.ArticlePubMedPMCPDF
• 3. Abdi J, Farhadi M, Aghace S, et al. Parasitic Contamination of Raw Vegetables in Iran: A Systematic Review and Meta-Analysis. J Med Sci 2014;14(3): 137−42. PMID: 10.3923/jms.2014.137.142.Article
• 4. Beaver PC, Snyder CH, Carrera GM, et al. Chronic eosinophilia due to visceral larva migrans Report of three cases. Pediatric 1952;9(1): 7−19.
• 5. Kroten A, Toczylowski K, Kiziewicz B, et al. Environmental contamination with Toxocara eggs and seroprevalence of toxocariasis in children of northeastern Poland. Parasitol Res 2016;115(1): 205−9. PMID: 10.1007/s00436-015-4736-0.ArticlePubMedPDF
• 6. Silva MB, Amor ALM, Santos LN, 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 2016;158−64. PMID: 27080332.Article
• 7. Akao N, Ohta N. Toxocariasis in Japan. Parasitol Int 2007;56(2): 87−93. PMID: 10.1016/j.parint.2007.01.009. PMID: 17317275.ArticlePubMed
• 8. Choi D, Lim JH, Choi DC, et al. Toxocariasis and ingestion of raw cow liver in patients with eosinophilia. Korean J Parasitol 2008;46(3): 139−43. PMID: 10.3347/kjp.2008.46.3.139. PMID: 18830052. PMID: 2553335.ArticlePubMedPMCPDF
• 9. Hoffmeister B, Glaeser S, Flick H, et al. Cerebral toxocariasis after consumption of raw duck liver. Am J Trop Med Hyg 2007;76(3): 600−2. PMID: 17360892.ArticlePubMed
• 10. Ebrahimifard F, Fakhar M, Sharif M, et al. Seroprevalence of Toxocara Infection among Adult Individuals with Eosinophilia in Babol, 2013. J Mazandaran Univ Med Sci 2015;25(121): 355−62.
• 11. Kyei G, Ayi I, Boampong JN, et al. Sero-epidemiology of Toxocara canis infection in children attending four selected health facilities in the central region of Ghana. Ghana Med J 2015;49(2): 77−83. PMID: 10.4314/gmj.v49i2.3. PMID: 26339090. PMID: 4549823.ArticlePubMedPMC
• 12. Romero Nunez C, Mendoza Martínez GD, Yañez Arteaga S, et al. Prevalence and risk factors associated with Toxocara canis infection in children. Scientific World Journal 2013;2013:572089PMID: 10.1155/2013/572089. PMID: 3690266.PubMedPMC
• 13. Won KY, Kruszon-Moran D, Schantz PM, et al. National seroprevalence and risk factors for zoonotic Toxocara spp. infection. Am J Trop Med Hyg 2008;79(4): 552−7. PMID: 18840743.ArticlePubMed
• 14. Mendonca LR, Figueiredo CA, Esquivel R, et al. Seroprevalence and risk factors for Toxocara infection in children from an urban large setting in Northeast Brazil. Acta Tropica 2013;128(1): 90−5. PMID: 10.1016/j.actatropica.2013.06.018. PMID: 23845771.ArticlePubMedPMC
• 15. Oliart-Guzmán H, et al. Epidemiology and control of child toxocariasis in the Western Brazilian Amazon–a population-based study. Am J Trop Med Hyg 2014;90(4): 670−81. PMID: 10.4269/ajtmh.13-0506. PMID: 24515946. PMID: 3973512.ArticlePubMedPMC
• 16. Taira K, Saeed I, Permin A, et al. Zoonotic risk of Toxocara canis infection through consumption of pig or poultry viscera. Vet Parasito 2004;121(1–2): 115−24. PMID: 10.1016/j.vetpar.2004.01.018.Article
• 17. Momeni T, Mahami-Oskouei E, Fallah A, Safaiyan L. Latent and asymptomatic Toxocara infection among young population in Northwest Iran: The necessity of informing people as a potential health risk. Scientifica 2016;2016:3562056PMID: 10.1155/2016/3562056. PMID: 27022503. PMID: 4789035.ArticlePubMedPMCPDF
• 18. Malla N, Aggarwal A, Mahajan R. A serological study of human toxocariasis in north India. Natl Med J India 2002;15(3): 145−7. PMID: 12186327.PubMed
• 19. Fan CK, Hung CC, Du WY, et al. Seroepidemiology of Toxocara canis infection among mountain aboriginal schoolchildren living in contaminated districts in eastern Taiwan. Trop Med Int Health 2004;9(12): 1312−8. PMID: 10.1111/j.1365-3156.2004.01332.x. PMID: 15598263.ArticlePubMed
• 20. Alonso JM, Bojanich MV, Chamorro M, Gorodner JO. Toxocara seroprevalence in children from a subtropical city in Argentina. Revista do Instituto de Medicina Tropical de São Paulo 2000;42(4): 235−7. PMID: 10.1590/S0036-46652000000400010.ArticlePDF
• 21. Chan PW, Anuar AK, Fong MY, et al. Toxocara seroprevalence and childhood asthma among Malaysian children. Pediatr In 2001;43(4): 350−3.Article
• 22. Sadjjadi SM, Khosravi M, Mehrabani D, Orya A. Seroprevalence of Toxocara infection in school children in Shiraz, Southern Iran. J Trop Pediatr 2000;46(6): 327−30. PMID: 10.1093/tropej/46.6.327.ArticlePubMedPDF
• 23. Ajayi OO, Duhlinska DD, Agwale SM, Njoku M. Frequency of human toxocariasis in Jos, Plateau state, Nigeria. Memórias do Instituto Oswaldo Cruz 2000;95(2): 147−9. PMID: 10.1590/S0074-02762000000200002.ArticlePDF
• 24. Habluetzel A, Traldi G, Ruggieri S, et al. An estimation of Toxocara canis prevalence in dogs, environmental egg contamination and risk of human infection in the Marche region of Italy. Vet Parasitol 2003;113(3–4): 243−52. PMID: 10.1016/S0304-4017(03)00082-7. PMID: 12719139.ArticlePubMed
• 25. Morimatsu Y, Akao N, Akiyoshi H, et al. A familial case of visceral larva migrans after ingestion of raw chicken livers: appearance of specific antibody in bronchoalveolar lavage fluid of the patients. Am J Trop Med Hyg 2006;75(2): 303−6. PMID: 16896137.ArticlePubMed

Figure & Data

References

Citations

Citations to this article as recorded by  

• Maternal COVID-19 infection and the fetus: Immunological and neurological perspectives
  Shahab Falahi, Amir Abdoli, Azra Kenarkoohi
  New Microbes and New Infections.2023; 53: 101135.     CrossRef
• Seroprevalence of Toxocariasis and Its Associated Risk Factors among Adult Population in Kavar District, Fars Province, South of Iran: A Cross-Sectional Community-Based Seroepidemiological Survey
  Fatemehsadat Pezeshkian, Ali Pouryousef, Mostafa Omidian, Fattaneh Mikaeili, Ali Reza Safarpour, Sara Shojaei-Zarghani, Bahador Sarkari, Payam Behzadi
  Interdisciplinary Perspectives on Infectious Disea.2023; 2023: 1.     CrossRef
• Seroprevalence and risk factors of Toxocara canis infection in children aged 2–15 years from the southwest Iran
  Masoud Foroutan, Shahrzad Soltani, Samaneh Bahadoram, Fatemeh Maghsoudi, Naser Kamyari, Shekoufe Haddadi
  Comparative Immunology, Microbiology and Infectiou.2022; 85: 101801.     CrossRef
• Seroprevalence of Toxocara spp. in children (3–13 years old) in Zahedan, Southeast of Iran
  Alireza Salimi Khorashad, Majid Shahraki, Mansour Rahmati Balaghaleh, Samaneh Abdolahi Khabisi, Sangeetha Rala, Reza Shafiei, Hadi Mirahmadi
  Journal of Parasitic Diseases.2021; 45(2): 449.     CrossRef
• The global prevalence of Toxocara spp. in pediatrics: a systematic review and meta-analysis
  Behnam Abedi, Mehran Akbari, Sahar KhodaShenas, Alireza Tabibzadeh, Ali Abedi, Reza Ghasemikhah, Marzieh Soheili, Shnoo Bayazidi, Yousef Moradi
  Clinical and Experimental Pediatrics.2021; 64(11): 575.     CrossRef
• Seroprevalence and associated risk factors of toxocariasis among nomads in Boyer-Ahmad County, southwest Iran
  Nasir Arefkhah, Mohammad Reza Shadzi, Fattaneh Mikaeili, Bahador Sarkari, Farideh Esfandiari, Fatemeh Goudarzi
  Transactions of The Royal Society of Tropical Medi.2020; 114(5): 372.     CrossRef
• Seroprevalence of anti-Toxocara antibody among multiple sclerosis patients: a case–control study
  Nastaran Khalili, Neda Khalili, Ali Nickhah, Bahman Khalili
  Journal of Parasitic Diseases.2020; 44(1): 145.     CrossRef
• Seroprevalence of toxocariasis and its related risk factors among municipal street sweepers in Shiraz District in Fars Province, southern Iran
  Amirhossein Erfani, Ali Pouryousef, Nasir Arefkhah, Reza Shahriarirad, Mohammad Rastegarian, Ali Zeighami, Fattaneh Mikaeili, Seyed Younes Hosseini, Bahador Sarkari
  Clinical Epidemiology and Global Health.2020; 8(2): 643.     CrossRef
• Toxocara infection: seroprevalence and associated risk factors among primary school children in central China
  Shuai Wang, Haoran Li, Zhijun Yao, Pengju Li, Dong Wang, Haizhu Zhang, Qing Xie, Zhenchao Zhang, Xiangrui Li
  Parasite.2020; 27: 30.     CrossRef
• Status of human toxocariasis, a neglected parasitic zoonosis in Iran: a systematic review from past to current
  Reza Shafiei, Mohammad T Rahimi, Reza Zolfaghari Emameh, Mehdi Mirzaei, Gregorio Perez-Cordon, Ehsan Ahmadpour
  Tropical Doctor.2020; 50(4): 285.     CrossRef