Risk Factors and Prevalence of Toxocariasis in Healthy Adults in South Khorasan Province, Eastern Iran

authors:

avatar Sanaz Ebrahimi ORCID 1 , avatar Amir Tavakoli Kareshk ORCID 1 , avatar Mohammad Darvishi ORCID 2 , avatar Nayereh Asadi ORCID 3 , avatar Vahid Bagheri ORCID 1 , avatar Gholamreza Barzegar ORCID 4 , avatar Rahmat Solgi ORCID 1 , *

Infectious Diseases Research Center, Birjand University of Medical Sciences, Birjand, Iran
Infectious Diseases and Tropical Medicine Research Center (IDTMRC), Department of Aerospace and Subaquatic Medicine, AJA University of Medical Sciences, Tehran, Iran
School of Nursing and Midwifery, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
Modern Care Journal: Vol.19, issue 3; e128079
published online: August 2, 2022
article type: Research Article
received: May 20, 2022
revised: July 4, 2022
accepted: July 6, 2022
DOI: https://doi.org/10.5812/modernc-128079

how to cite: Ebrahimi S, Tavakoli Kareshk A, Darvishi M, Asadi N, Bagheri V , et al. Risk Factors and Prevalence of Toxocariasis in Healthy Adults in South Khorasan Province, Eastern Iran. Mod Care J. 2022;19(3):e128079. https://doi.org/10.5812/modernc-128079.

Abstract

Background:

Toxocariasis is a common zoonotic helminthic disease with worldwide distribution. Seroepidemiological data related to human toxocariasis and its risk factors are limited in the east of Iran.

Objectives:

The current study evaluated the seroprevalence of toxocariasis and associated risk factors in clinically healthy individuals aged 18 years or older in eastern Iran.

Methods:

We took 450 samples from clinically healthy individuals referred to medical laboratories for health screening between March and May 2022 in Birjand, Iran. The seroprevalence of IgG antibody against Toxocara was performed using the enzyme-linked immunosorbent assay (ELISA) kit (IBL, Germany). Logistic regression was used to analyze the association between toxocariasis and potential risk factors by SPSS 21.0 software. A probability P value less than 0.05 was considered statistically significant.

Results:

The sample included 210 (56.6%) men, and 240 women (53.3%) who were aged 18 to 81 years (mean 35 ± 13 years). The Toxocara ELISA was positive in 36 (8%) individuals. The statistical analysis showed that washing hands before eating (odds ratio (OR) = 0.1, 95% CI: 0.05 - 0.3, P < 0.0001), contact with cats and dogs (OR = 0.1, 95% CI: 0.05 - 0.3, P < 0.00001), and raw meat consumption (OR = 4.8, 95% CI: 2.2 - 11.4), P < 0.0004) were risk factors associated with Toxocara infection.

Conclusions:

The relatively low seroprevalence of Toxocara infection in our study can be caused by environmental and socio-cultural conditions and moderate to high hygiene standards in Birjand. It is suggested that more extensive studies be conducted with larger sample sizes in at-risk groups in this area.

1. Background

Toxocariasis is a common zoonotic helminthic disease primarily distributed in subtropical and tropical regions (1). Humans can be infected with toxocariasis by ingesting soil and vegetables contaminated with the eggs of Toxocara canis or Toxocara cati. In some cases, the infection can be acquired by direct contact of hands with the hair of dogs or, in rare cases, via the consumption of larvae in the raw meat of Toxocara-infected paratenic hosts.

Humans are accidental hosts for toxocariasis. The parasite can complete its life cycle in humans. Therefore, eggs are not excreted in human fecal samples (2). Human toxocariasis, in most cases, is clinically asymptomatic. Clinical manifestations of toxocariasis include visceral larva migrans (VLM), ocular larva migrans (OLM), and covert and atypical toxocariasis according to the affected organ (3). The diagnosis of human toxocariasis is performed mainly by a combination of clinical examination and enzyme-linked immunosorbent assay (ELISA) for the excretion-secretion antigen (4).

Seroprevalence varies from as low as 1% in Spain to 86% in Santa Lucia, with a tropical climate (5). Based on seroprevalence studies, toxocariasis is more prevalent in socioeconomically poor children in tropical and subtropical regions. The seroprevalence of human toxocariasis is predominant in people under 20 years and urban regions in different parts of Iran. The prevalence of human toxocariasis with overall 28 records from all over Iran was reported as 9.3% (95% CI: 6.3 - 13.1%) (6).

Several risk factors are related to the prevalence of Toxocara infection in humans, such as keeping cats and dogs and raw consumption of vegetables (7).

2. Objectives

However, sero-epidemiological data related to human toxocariasis and its risk factors are limited in eastern Iran. Therefore, we studied the seroprevalence of human toxocariasis and associated risk factors among clinically healthy individuals in Birjand district, eastern Iran, for the first time. This study aimed to attract public attention to Toxocara infection in the country’s eastern regions, especially South Khorasan province.

3. Methods

3.1. Study Location and Patient Selection

A cross-sectional study was performed in Birjand, Iran. South Khorasan province is located in the east part of Iran, on the border with Afghanistan, with a predominant desert climate (8). According to a 25% infection prevalence in a previous study (9), the sample size was calculated as follows:

n=z21-a2×p 1-pd2
n=1.962×0.20 (1-0.20)0.0016≈400

In order to adjust for missing data, the sample size was increased to 450 people selected from clinically healthy individuals between March and May 2022. The healthy subjects above 18 years old who were voluntarily admitted to hospitals for health screening were regarded as clinically healthy individuals. The exclusion criteria were hemolyzed samples and infection with other intestinal parasites.

3.2. Data Collection

A questionnaire was used to collect risk factors and epidemiological data (age, gender, residential area, washing hands before eating, consuming raw/undercooked meat and vegetables, and contacting cats and dogs). The content validity of this questionnaire was checked and confirmed by experts. The reliability of the questionnaire was also confirmed owing to the questions’ objectiveness and frequent use in previous studies.

3.3. Sampling and Laboratory Analysis

Approximately 5 mL of blood was collected from each participant in a clot activator tube. The collected sera were stored at -20°C until testing. The IgG antibodies against Toxocara were detected by T. canis excretory-secretory (TES) antigens using a commercial ELISA kit (IBL, manufactured in Hamburg, Germany) following the manufacturer’s instructions. Briefly, serum samples were incubated and conjugated with alkaline phosphatase, followed by the tetramethylbenzidine (TMB) substrate.

Absorbance readings were performed at 450 nm. The average absorbance reading for three negative control sera plus two standard deviations was considered a cutoff value. The OD values ≥ 0.3 were reported positive.

3.4. Statistical Analysis

Frequency analysis was performed to describe the participants’ characteristics and the parasite prevalence. Logistic regression was used to analyze the association between toxocariasis and potential risk factors by SPSS 21.0 software. Odds ratios (ORs) were considered statistically significant if the 95% CI did not include one. A probability P value less than 0.05 was considered statistically significant.

4. Results

A total of 450 clinically healthy individuals (210 men and 240 women) aged 18 to 81 years (mean 35 ± 13 years) were randomly referred to medical laboratories for health screening in Birjand, Iran. Table 1 shows the demographic characteristics of the sample. The majority (28.8%) of individuals were in the age range of 21 - 30 years. The Toxocara ELISA was positive in 36 (8%) of the 450 individuals. The highest prevalence rate of toxocariasis was reported in individuals over 61 years old (14.2%, 95% CI 0.3 - 12.9) (Table 1). Moreover, statistical analysis showed that washing hands before eating (OR = 0.1, 95% CI 0.05 - 0.3), P < 0.0001), contact with cats and dogs (OR = 0.1, 95% CI 0.05 - 0.3, P < 0.00001), and raw meat consumption (2.2 - 11.4) (OR = 4.8, 95% CI 2.2 - 11.4), P < 0.0004) were risk factors associated with Toxocara infection. However, there were no relationships between toxocariasis and age, gender, residency, and raw vegetable intake.

Table 1.

Odds Ratios of Risk Factors Associated with Seropositivity to Toxocariasis in the Study Population in Birjand, Iran

CharacteristicsNumber (n)Seropositive, No. (%)Odds Ratio (95% CI)P Value
Age
≤ 20554 (7.25)Reference
21 - 3013010 (7.6)1.06 (0.3 - 3.5)0.9
31 - 401029 (8.8)1.2 (0.3 - 4.2)0.7
41 - 50997 (6)0.9 (0.2 - 3.4)0.9
51 - 60404 (10)1.4 (0.3 - 6)0.6
≥ 61142 (14.2)2.1 (0.3 - 12.9)0.4
Gender
Male 24022 (9.1)Reference0.3
Female 21014 (6.6)0.7 (0.3 - 1.4)
Washing hands before eating
No 19030 (15.7)Reference
Yes 2606 (2.3)0.1 (0.05 - 0.3)< 0.0001
Contact with dog and cat
No2908 (2.7)Reference
Yes16028 (17.5)7.4 (3.3 - 16.8)< 0.00001
Residency
Urban 28518 (5.9)Reference
Rural 16518 (11.5)1.8 (0.91 - 3.59)0.08
Raw vegetable consumption1.2 (0.6 - 2.5)0.53
Yes 11012 (10.9)1.6 (0.7 - 3.4)0.1
No32022 (6.8)Reference
Raw meat consumption
Yes519 (17.6)4.8 (2.2 - 11.4)0.0004
No 39917 (4.2)Reference

5. Discussion

The current study evaluated the seroprevalence of toxocariasis among clinically healthy individuals and potential factors associated with Toxocara infection in South Khorasan province, eastern Iran. The prevalence of toxocariasis among asymptomatic individuals worldwide varies from 2% to 80% (10). Many factors, such as lifestyle, geographical conditions, and detection methods, play a role in such differences. Moreover, the seroprevalence of anti-Toxocara IgG antibodies was significantly lower in the present study than in previous studies in Peru (44.92%) (11), United States (13.9%) (12), Brazil (51.6%) (13), and South Korea (51.2%) (14). The prevalence of anti-Toxocara IgG was higher in the current study than in the same study from Denmark (2.4%) (15) and approximately consistent with an Egyptian study (7.7%) (16). In this study, the overall seroprevalence of IgG antibodies against toxocariasis was 8%, slightly lower than the mean value (9%) of previous studies conducted in different parts of Iran (6, 17). In a previous study performed in Iran, 49 (15.54 %) healthy people were seropositive for toxocariasis, and a significant risk factor was contact with cats and dogs but not age and gender (18), while in the current study, the seroprevalence was 8% and a significant risk factor was washing hands before eating, contact with cats and dogs, and raw meat consumption. In the current study, seroprevalence increased along with age but was not associated with gender, residency, or raw vegetable intake. In the present study, the seroprevalence was increased with age, consistent with those reported previously (12, 14). In this study, there was no statistically significant association between toxocariasis and age, gender, residency, and raw vegetable intake.

We observed no statistically significant association between Toxocara infection seropositivity and age, gender, residency, and raw vegetable intake. However, in contrast to some studies (19, 20), we found that contact with a dog or cat could be a risk factor for Toxocariasis. In the present study, the prevalence was higher in men than women, but this difference was not statistically significant. To our knowledge, the past epidemiological studies regarding sero-epidemiological data related to human toxocariasis and its risk factors are limited in the east of Iran.

5.1. Conclusions

This study’s relatively low seroprevalence of toxocariasis can be due to environmental conditions and relatively good health status in Birjand. It is suggested that more extensive studies be conducted with larger sample sizes in at-risk groups in this area.

Acknowledgements

References

  • 1.

    Chen J, Zhou DH, Nisbet AJ, Xu MJ, Huang SY, Li MW, et al. Advances in molecular identification, taxonomy, genetic variation and diagnosis of Toxocara spp. Infect Genet Evol. 2012;12(7):1344-8. [PubMed ID: 22569289]. https://doi.org/10.1016/j.meegid.2012.04.019.

  • 2.

    Hashemi SM, Mahmoodi S, Mehravaran A, Mirahmadi H, Khabisi S, Alijani E, et al. Serological and molecular evaluation of toxoplasmosis in patient undergoing chemotherapy for malignancies in southeast of Iran. Gene Rep. 2021;23:101163. https://doi.org/10.1016/j.genrep.2021.101163.

  • 3.

    Fan CK, Liao CW, Cheng YC. Factors affecting disease manifestation of toxocarosis in humans: genetics and environment. Vet Parasitol. 2013;193(4):342-52. [PubMed ID: 23290279]. https://doi.org/10.1016/j.vetpar.2012.12.030.

  • 4.

    Cong W, Zhang XX, Zhou N, Yu CZ, Chen J, Wang XY, et al. Toxocara seroprevalence among clinically healthy individuals, pregnant women and psychiatric patients and associated risk factors in Shandong Province, Eastern China. PLoS Negl Trop Dis. 2014;8(8). e3082. [PubMed ID: 25101756]. [PubMed Central ID: PMC4125144]. https://doi.org/10.1371/journal.pntd.0003082.

  • 5.

    Alderete JM, Jacob CM, Pastorino AC, Elefant GR, Castro AP, Fomin AB, et al. Prevalence of Toxocara infection in schoolchildren from the Butanta region, Sao Paulo, Brazil. Mem Inst Oswaldo Cruz. 2003;98(5):593-7. [PubMed ID: 12973524]. https://doi.org/10.1590/s0074-02762003000500002.

  • 6.

    Eslahi AV, Badri M, Khorshidi A, Majidiani H, Hooshmand E, Hosseini H, et al. Prevalence of Toxocara and Toxascaris infection among human and animals in Iran with meta-analysis approach. BMC Infect Dis. 2020;20(1):20. [PubMed ID: 31910815]. [PubMed Central ID: PMC6947998]. https://doi.org/10.1186/s12879-020-4759-8.

  • 7.

    Momeni T, Mahami-Oskouei M, Fallah E, Safaiyan A, Mahami-Oskouei L. Latent and Asymptomatic Toxocara Infection among Young Population in Northwest Iran: The Necessity of Informing People as a Potential Health Risk. Scientifica (Cairo). 2016;2016:3562056. [PubMed ID: 27022503]. [PubMed Central ID: PMC4789035]. https://doi.org/10.1155/2016/3562056.

  • 8.

    Karamian M, Haghighi F, Hemmati M, Taylor WR, Salehabadi A, Ghatee MA. Heterogenity of Echinococcus canadensis genotype 6 - the main causative agent of cystic echinococcosis in Birjand, Eastern Iran. Vet Parasitol. 2017;245:78-85. [PubMed ID: 28969842]. https://doi.org/10.1016/j.vetpar.2017.08.018.

  • 9.

    Sharif M, Daryani A, Barzegar G, Nasrolahei M, Khalilian A. Seroprevalence of toxocariasis in schoolchildren in Northern Iran. Pak J Biol Sci. 2010;13(4):180-4. [PubMed ID: 20437685]. https://doi.org/10.3923/pjbs.2010.180.184.

  • 10.

    Pawlowski Z. Toxocariasis in humans: clinical expression and treatment dilemma. J Helminthol. 2001;75(4):299-305. [PubMed ID: 11818044]. https://doi.org/10.1017/s0022149x01000464.

  • 11.

    Roldan WH, Espinoza YA, Huapaya PE, Huiza AF, Sevilla CR, Jimenez S. Frequency of human toxocariasis in a rural population from Cajamarca, Peru determined by DOT-ELISA test. Rev Inst Med Trop Sao Paulo. 2009;51(2):67-71. [PubMed ID: 19390733]. https://doi.org/10.1590/s0036-46652009000200002.

  • 12.

    Won KY, Kruszon-Moran D, Schantz PM, Jones JL. National seroprevalence and risk factors for Zoonotic Toxocara spp. infection. Am J Trop Med Hyg. 2008;79(4):552-7. [PubMed ID: 18840743].

  • 13.

    Colli CM, Rubinsky-Elefant G, Paludo ML, Falavigna DL, Guilherme EV, Mattia S, et al. Serological, clinical and epidemiological evaluation of toxocariasis in urban areas of south Brazil. Rev Inst Med Trop Sao Paulo. 2010;52(2):69-74. [PubMed ID: 20464126]. https://doi.org/10.1590/s0036-46652010000200002.

  • 14.

    Lee JY, Yang MH, Hwang JH, Kang M, Paeng JW, Yune S, et al. The Prevalence of Toxocariasis and Diagnostic Value of Serologic Tests in Asymptomatic Korean Adults. Allergy Asthma Immunol Res. 2015;7(5):467-75. [PubMed ID: 26122506]. [PubMed Central ID: PMC4509659]. https://doi.org/10.4168/aair.2015.7.5.467.

  • 15.

    Stensvold CR, Skov J, Moller LN, Jensen PM, Kapel CM, Petersen E, et al. Seroprevalence of human toxocariasis in Denmark. Clin Vaccine Immunol. 2009;16(9):1372-3. [PubMed ID: 19641098]. [PubMed Central ID: PMC2745020]. https://doi.org/10.1128/CVI.00234-09.

  • 16.

    El-Shazly AM, Abdel Baset SM, Kamal A, Mohammed KA, Sakrs TI, Hammad SM. Seroprevalence of human toxocariasis (visceral larva migrans). J Egypt Soc Parasitol. 2009;39(3):731-44. [PubMed ID: 20120741].

  • 17.

    Zibaei M, Sadjjadi SM, Sarkari B, Uga S. Evaluation of Toxocara cati Excretory-Secretory Larval Antigens in Serodiagnosis of Human Toxocariasis. J Clin Lab Anal. 2016;30(3):248-53. [PubMed ID: 25846840]. [PubMed Central ID: PMC6807093]. https://doi.org/10.1002/jcla.21844.

  • 18.

    Raissi V, Sohrabi Z, Getso M, Raiesi O, Hashemi Hafshejani S, Shabandoust H, et al. Risk factors and prevalence of toxocariasis in pregnant women and diabetic patients compared to healthy adults in Ilam province, western Iran. EXCLI J. 2018;17:983-8. [PubMed ID: 30564078]. [PubMed Central ID: PMC6295622]. https://doi.org/10.17179/excli2018-1630.

  • 19.

    Gabrielli S, Tasic-Otasevic S, Ignjatovic A, Fraulo M, Trenkic-Bozinovic M, Momcilovic S, et al. Seroprevalence and Risk Factors for Toxocara canis Infection in Serbia During 2015. Foodborne Pathog Dis. 2017;14(1):43-9. [PubMed ID: 27893948]. https://doi.org/10.1089/fpd.2016.2190.

  • 20.

    Lotsch F, Obermuller M, Mischlinger J, Mombo-Ngoma G, Groger M, Adegnika AA, et al. Seroprevalence of Toxocara spp. in a rural population in Central African Gabon. Parasitol Int. 2016;65(6 Pt A):632-4. [PubMed ID: 27594568]. https://doi.org/10.1016/j.parint.2016.09.001.