Epidemiological, clinical and laboratory features of ...

ORIGINAL ARTICLE

Trans R Soc Trop Med Hyg 2018; 112: 255–263 doi:10.1093/trstmh/try051 Advance Access publication 16 June 2018

Epidemiological, clinical and laboratory features of toxocariasis in school children from Aragua State, Venezuela María Martíneza,b, Jesica Monteroa, Adriana Pinedaa, Víctor Mijaresa, María Laresb, Emily Catalanob and Elizabeth Ferrera,b,* a Departamento de Parasitología, Facultad de Ciencias de la Salud, Universidad de Carabobo Sede Aragua, Maracay, estado Aragua, Venezuela; bInstituto de Investigaciones Biomédicas ‘Dr. Francisco J. Triana Alonso’ (BIOMED) Universidad de Carabobo Sede Aragua, Maracay, estado Aragua, Venezuela

*Corresponding author: Tel: +58–243-2425822; Fax: +58–243-2425333; E-mail: [email protected]

Received 3 January 2018; revised 28 April 2018; editorial decision 15 May 2018; accepted 15 May 2018 Background: Toxocariasis is a widespread zoonosis caused by canine and feline Toxocara spp. In Venezuela, seroepidemiological studies in Aragua State have been carried out only in preschool children. The objective of this study was to determine the prevalence of anti-Toxocara spp. antibodies and identify clinical symptoms and risk factors of Toxocara spp. infection in school children in two municipalities of Aragua State of Venezuela. Methods: A cross-sectional field study with 259 children between 6 and 12 y of age was conducted in six schools in Aragua State. Immunoglobulin G antibodies against Toxocara spp. by enzyme-linked immunosorbent assay, haematology and eosinophil counts were detected in blood. Participating families filled in a questionnaire and studied children were clinically evaluated by paediatricians. Results: Anti-Toxocara spp. antibodies were detected in 14.3% of children. The seroprevalence in the schools studied ranged from 4.4% to 24.1%. Statistical associations with eosinophilia, decreased visual acuity, eyestrain, headache and paleness were found. Significant risk factors were contact with dogs, playing with dogs and playing with soil. Conclusions: The identification of risk factors and their association with infection suggest that the infection is a problem in the municipalities studied, so screening for toxocariasis in school children should be recommended. Keywords: diagnosis, epidemiology, risk factors, seroprevalence, Toxocara spp., toxocariasis

Introduction Toxocara spp. are intestinal parasites of dogs, cats and other species. In humans, toxocariasis is a soil-transmitted zoonosis caused by infection with larvae of canine and feline Toxocara spp., which are unable to complete development. The parasite can cause four syndromes: visceral larva migrans (VLM), ocular larva migrans (OLM), covert/common toxocariasis (mostly asymptomatic or with very few symptoms), cerebral toxocariasis and neurotoxocariasis. Visceral larva migrans occurs when the immune system produces an inflammatory reaction around the parasite, forming granulomas in various organs. Common symptoms of the acute phase of infection are weakness, fever and malaise, while others symptoms depend on the location of the larvae. Ocular larva migrans can lead to visual loss, while neurotoxocariasis has

been associated with reduced cognitive functions in children and young adults. The relation with asthma in children has been described in the recent years. The main haematological characteristics of toxocariasis are eosinophilia and leucocytosis, occurring most commonly in the acute phase of infection.1–10 The diagnosis of toxocariasis in humans is difficult due to non-specific symptoms, detection of the parasites by coproparasitology tests is not possible because of the incomplete parasite life cycle and identification of larvae in tissues by biopsy is an invasive procedure. Thus the diagnosis takes into account epidemiological data, clinical symptoms, haematological findings and serological titration of antibodies against secreted/excreted antigens of larvae of Toxocara spp. Antibodies against Toxocara spp. are usually measured by enzyme-linked immunosorbent assay (ELISA) and less frequently by western blot.1–3

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M. Martínez et al.

The principal risk factors are related with socio-economic conditions, age and contact with parasite embryonated eggs. Another factor that modulates the transmission of toxocariasis is climate, since the highest seroprevalence rates of toxocariasis have been found in wet and warm areas.2–4,11 Toxocariasis is endemic in Latin America, Africa and Asia. The prevalence of human infection ranges from 1.8% to 78% worldwide and in Latin America from 2.5% to 68.6%.11,12 In Venezuela the prevalence of toxocariasis is unknown. Several studies report the seroprevalence of Toxocara spp. antibodies at 9.7% to 66.6% in 8 of 23 states.13–17 In the Aragua State, there is little information available about toxocariasis; only one published study has been made in preschool children by our group.17 In order to complement the data about toxocariasis in the Aragua State of Venezuela, we conducted the present study in school children in two of the previously studied municipalities of Aragua State.

Methods Study area The area of study included two municipalities of Aragua State, Venezuela, where an epidemiological study was conducted in six schools. The municipalities studied were Santiago Mariño, situated at 10°13′N and 67°28′W, at an altitude of 468 m, with an approximate area of 536 km2 (school 1, La Ganadería; school 2, Algeria Laya; school 3, Ivonne González) and Francisco Linares Alcántara, situated at 10°12′N and 67°34′W longitude, at an altitude of 428 m, with an approximate area of 238 km2 (school 4, Reina de Vásquez; school 5, Francisco de Miranda; school 6, Santiago Mariño) (Table 1, Figure. 1). The climate of the study area is wet and warm, with an annual average temperature of 25 ± 2°C with a rainy season (May–October) and a dry season (November–April) and precipitation of 900–1000 mm annually.18

Population and sample collection The study population included 36 286 boys and girls between 6 and 12 y of age. The number of children in this study was estimated to include a minimum sample size of 218 individuals, allowing for a 10% loss of enrolled participants. This calculation is based on a prevalence of infection of at least 29% for the total population, according to a seroepidemiological study done in preschool children.17 The sample was selected by simple random cluster sampling (one conglomerate equal to one school) to reach the estimated size. The selection criteria for individuals included in the study were registration at the selected institution, age between 6 and 12 y and written authorization by parents or guardians.

housing conditions, soil playing habits, geophagia, hand washing, contact with dogs and socio-economic status according to the Graffar–Méndez–Castellano method.19 Following the Graffar method, modified for Venezuela by Mendez, an index was used to classify the population into five strata: high, upper middle, middle, relative poverty and critical poverty. This index is based on a compilation of the following measures: family income, parent’s education level, profession of the head of the family and housing conditions.19 All the studied children were clinically evaluated by paediatricians from our working group and the signs and symptoms found were included in the questionnaires. A sample of 7 mL of blood was collected from each individual; 3.5 mL of blood were centrifuged at 2500 rpm for 10 min to obtain serum, which was stored at −20°C. The remaining 3.5 mL was treated with ethylenediaminetetraacetic acid for automated haematological assay using a Celldyn 1700 analyser (Abbott, Abbott Park, IL, USA) and a manual eosinophils count using a haemocytometer.

Detection of anti-Toxocara spp. immunoglobulin G (IgG) antibodies against excreted/secreted antigens Anti-Toxocara spp. IgG antibodies against excreted/secreted antigens were determined using a previously reported standardized and validated ELISA.20 The ELISA was evaluated with serum samples from patients with confirmed toxocariasis (n=17); patients with other helminth infections (n=48) such as ascariasis (n=9), trichuriasis (n=7), enterobiasis (n=5), hookworm (n=5), strongyloidiasis (n=4), schistosomiasis (n=3), taeniasis (n=3), cysticercosis (n=5), hymenolepiasis (n=3), hidatidosis (n=2) and onchocerciasis (n=2); and healthy individuals (n=40). The diagnostic indexes of the standardized ELISA were sensitivity 100%, specificity 99%, positive predictive value 94% and negative predictive value 100%. These diagnostic indexes indicate that the ELISA using excreted/ secreted antigens of Toxocara canis was suitable for immunodiagnosis of human toxocariasis. In order to confirm the specificity of T. canis excreted/secreted antigens before use in the ELISA for diagnosis, they were was also evaluated by western blotting, as previously reported.21 Conditions for western blots were standardized and the presence of antibodies in sera from individuals with toxocariasis (n=30), individuals with other parasitic infections (n=20) and healthy individuals (n=20) was determined using the prepared T. canis excreted/secreted antigens. Western blot analysis identified immunodominant bands only in sera from individuals with toxocariasis, while patients with other parasitic diseases and healthy individuals did not have detectable bands using these antigens. Antibody titres against Toxocara spp. were determined since both dogs and cats coexist in the same environment and the antigens prepared from T. canis could potentially cross-react with Toxocara cati antigens.

Socioepidemiological data and blood samples collection

Statistical analysis

Parents or guardians of participating children were required to fill out a standardized and validated questionnaire. The questionnaires were designed to collect epidemiological and clinical data concerning exposure to and infection with Toxocara spp., including the type of residence, school location and facilities,

Data were recorded using Excel 2010 (Microsoft, Redmond, WA, USA) and analysed with the Epi Info 6 (Centers for Disease Control, Atlanta, GA, USA) and Stata 10.0 (StataCorp, College Station, TX, USA) statistical software packages. The frequency distribution and other statistical measurements were calculated


Transactions of the Royal Society of Tropical Medicine and Hygiene

Table 1. Seroprevalence of toxocariasis by municipality, educational institution, gender and age and their association with the presence of antibodies anti-Toxocara spp. in children from two municipalities of Aragua State, Venezuela Location

Participants Municipality Santiago Mariñoa Francisco Linares Alcántara School 1, La Ganaderíaa,b,d 2, Argelia Layac,d 3, Ivonne Gonzálezc,d 4, Reina de Vásquezc,e 5, Francisco de Mirandac,e 6, Santiago Mariñoc,e Gender Femalea Male Age (y) 6a 7 8 9 10 11–12 a

Total, n (%)

Antibodies anti-Toxocara spp.

p-Value

Positive, n (%)

Negative, n (%)

OR (95% CI)

259 (100)

37 (14.3)

222 (85.7)

110 (42.5) 149 (57.5)

9 (8.2) 28 (18.8)

101 (91.8) 121 (81.2)

1.0 (–) 2.6 (1.2 to 5.8)

– 0.016

36 (13.9) 28 (10.8) 46 (17.8) 58 (22.4) 58 (22.4) 33 (12.7)

3 (8.3) 4 (14.3) 2 (4.4) 7 (12.1) 14 (24.1) 7 (21.2)

33 (91.7) 24 (85.7) 44 (95.6) 51 (87.9) 44 (75.9) 26 (78.8)

1.0 (–) 1.8 (0.4 to 9.0) 0.5 (0.1 to 3.2) 1.5 (0.4 to 6.3) 3.5 (0.9 to 13.2) 3.0 (0.7 to 12.6)

– 0.454 0.462 0.570 0.064 0.141

148 (57.1) 111 (42.9)

16 (10.8) 21 (18.9)

132(89.2) 90 (81.1)

1.0 (–) 0.5 (0.3 to 1.0)

– 0.068

70 (27.0) 32 (12.4) 42 (16.2) 33 (12.7) 52 (20.1) 30 (11.6)

8 (11.4) 4 (12.5) 9 (21.4) 4 (12.1) 9 (17.3) 3 (10.0)

62 (88.6) 28 (87.5) 33 (78.6) 29 (87.9) 43 (82.7) 27 (90.0)

1.00 (–) 1.1 (0.3 to 4.0) 2.1 (0.7 to 6.0) 1.1 (0.3 to 3.8) 1.6 (0.6 to 4.5) 0.9 (0.2 to 4.1)

– 0.876 0.159 0.919 0.357 0.834

Reference category. bRural. cUrban. dSantiago Mariño. eFrancisco Linares Alcántara.

Figure 1. Map of Venezuela highlighting the Aragua State and the municipalities of Aragua State that were studied.


M. Martínez et al.

for all collected variables. Seroprevalence was related to the age, gender and residence of each child using frequency distribution, percentages and cross tabulation. Subsequently the relationship of seropositive and seronegative individuals with the studied variables was analysed. Categorical variables were analysed using odds ratios (ORs) and proof of partnership derived using a χ2 distribution or Fisher’s exact two-tailed test. Continuous study variables were compared with a

Student’s t test. The significance level for all statistical tests was 0.05.

Ethical considerations The project was approved by the Committee of Bioethics at the Institute of Biomedical Research of the University of Carabobo (BIOMED-UC), following the guidelines for humans and animal

Table 2. Clinical and haematological characteristics and their association with the presence of antibodies anti-Toxocara spp. in the studied children from two municipalities of Aragua State, Venezuela Total, n (%)

Participants Symptoms Blurred vision Decreased visual acuity Epiphora Eyestrain Ocular pain Endotropia Photophobia Headache Hacking cough Productive cough Respiratory distress Allergic reactions Cutaneous/mucosal pallor Fever Abdominal pain Hepatomegaly Seizures Irritability Pruritus Arthralgia/myalgia Hyporexia Nausea/vomiting Palpitations Laboratory Anaemia Leucocytosis Eosinophilia

a

p-Value

Positive, n (%)

Negative, n (%)

259 (100)

37 (14.3)

222 (85.7)

21 (8.1) 11 (4.3) 6 (2.3) 15 (5.8) 7 (2.7) 1 (0.4) 4 (1.5) 37 (14.3) 30 (11.6) 20 (7.7) 8 (3.1) 11 (4.3) 10 (3.9) 12 (4.6) 26 (10.0) 2 (0.8) 4 (1.5) 3 (1.2) 4 (1.5) 16 (6.2) 6 (2.3) 3 (1.2) 4 (1.5)

5 (13.5) 4 (10.8) 2 (5.4) 5 (13.5) 1 (2.7) 0 (0.0) 2 (5.4) 10 (27.0) 5 (13.5) 4 (10.8) 1 (2.7) 2 (5.4) 5 (13.5) 3 (8.1) 6 (16.2) 1 (2.7) 0 (0) 1 (2.7) 0 (0) 5 (13.5) 2 (5.4) 1 (2.7) 2 (5.4)

16 (7.2) 7 (3.2) 4 (1.8) 10 (4.5) 6 (2.7) 1 (0.5) 2 (0.9) 27 (12.2) 25 (11.3) 16 (7.2) 7 (3.2) 9 (4.1) 5 (2.3) 9 (4.1) 20 (9.0) 1 (0.5) 4 (1.8) 2 (0.9) 4 (1.8) 11 (5.0) 4 (1.8) 2 (0.9) 2 (0.9)

2.0 (0.6 to 5.8) 3.7 (1.0 to 13.4) 3.1 (0.5 to 17.6) 3.3 (1.0 to 10.3) 1.0 (0.11 to 8.5) –a 6.2 (0.8 to 46.0) 2.6 (1.1 to 6.1) 1.2 (0.4 to 3.4) 1.5 (0.4 to 4.9) 0.8 (0.1 to 7.1) 1.3 (0.2 to 6.5) 6.7 (1.8 to 24.7) 2.0 (0.5 to 8.1) 1.9 (0.7 to 5.2) 6.1 (0.3 to 100) –a 3.0 (0.2 to 34.5) –a 2.9 (0.9 to 9.1) 3.1 (0.5 to 17.6) 3.0 (0.2 to 34.5) 6.2 (0.8 to 46.0)

0.201 0.044 0.199 0.039 1.000 – 0.071 0.020 0.692 0.450 0.884 0.707 0.004 0.287 0.183 0.203 – 0.367 – 0.055 0.199 0.367 0.071

18 (7.0) 10 (3.9) 52 (20.1)

3 (8.1) 2 (5.4) 12 (32.4)

15 (6.8) 8 (3.6) 40 (18.0)

1.2 (0.3 to 4.4) 1.5 (0.3 to 7.4) 2.2 (0.9 to 5.1)

0.765 0.601 0.043

Laboratory Absolute value

Haemoglobin (mmol/L)* Haematocrit (%)b Leucocytes (×109/L)** Eosinophils (%)c Eosinophils (×109/L)***

Antibodies anti-Toxocara spp. OR (95% CI)

IgG antibodies anti-Toxocara spp. Sample mean

Positive, mean

Negative, mean

Mean difference (95% CI)

p-Value

7.6 39.0 7.39 4.5 0.35

7.8 39.5 7.7 5.9 0.46

7.6 38.9 7.3 4.2 0.33

−0.3 (−6.4 to 0.2) −0.6 (−1.4 to 0.0) −0.32 (−1.11 to 0.46) −1.6 (−3.1 to 0.1) −0.14 (−0.25 to 0.03)

0.035 0.079 0.419 0.027 0.012

Uncalculated. Reference values: b37–47%. c1–4%. *7.45–11.17 mmol/L, **4.5–11.5 × 109/L, ***0.06–0.5 × 109/L.



care by the Commission of Bioethics of the Ministry of Science and Technology and the Operational Guidelines for Ethics Committees that Review Biomedical Research (TDR/PRD/ETHICS/ 2000.1). An informed consent was obtained from parents or guardians of participating children for obtaining blood samples according to ethical rules. All participants received complete medical care and children were given antiparasitics and specific treatments for other diseases as required.

Results Detection of anti-Toxocara spp. IgG antibodies against excreted/secreted antigens This study included 259 children, of whom 57.1% (148/259) were female and 42.9% (111/259) were male, with an age range of 6–12 y. Most of the participants were from Francisco Linares Alcántara (57.5% [149/259]) (Table 1). Sera from 14.3% (37/259) of children were positive for antibodies anti-Toxocara spp. excreted/secreted antigens by ELISA. Seroprevalence was greater for males (18.9% [21/111]) than for females (10.8% [16/148]), with no statistically significant association (p=0.068). Regarding age, seroprevalence was higher in children who were 8 y of age (21.4% [9/42]) and lower in children 11–12 y of age (10.0% [3/30]), with no statistically significant association (Table 1). The highest seroprevalence was found in Francisco Linares Alcántara (18.8% [28/149]) and seropositivity in Santiago Mariño was significantly lower (8.2% [9/110]) (OR 2.6 [95% confidence interval {CI} 2.3 to 4.6], p=0.016) (Table 1). The highest seroprevalence was in school 5, with 24.1% (14/58) seropositivity (OR 3.5 [95% CI 0.9 to 13.2], p=0.064) and the lowest was in the school 3, with 4.4% (2/46) (OR 0.5 [95% CI 0.1 to 3.2], p=0.46). Seroprevalence in schools 1, 2, 4 and 6 was lower compared with school 5, but not statistically significant (Table 1).

Clinical and laboratory data Clinical manifestations in 6- to 12-year-old children and their association with the presence of antibodies against Toxocara spp. are shown in Table 2. The predominant clinical signs and symptoms in individuals with antibodies against Toxocara spp. were headache (27.0% [10/37]) and cutaneous/mucosal pallor (13.5% [5/37]), with a statistically significant association. Others signs and symptoms were important, including abdominal pain, hacking cough and arthralgia/myalgia, but with no statistically significant association. Ocular symptoms such as blurred vision and eye pain were reported infrequently but were more frequently observed in seropositive than in seronegative individuals, although no statistically significant associations were observed, while decreased visual acuity and eyestrain had a statistically significant association. Other signs and symptoms recorded in Table 2 showed no clear indication of any association with seropositivity. The mean haemoglobin (Hb) in children with antibodies against Toxocara spp. was 7.8 mmol/L and was 7.6 mmol/L in seronegative individuals (p=0.035) (Table 2). A total of 7% (18/ 259) of the children studied had anaemia (Hb 11.5 × 109/L), without a significant difference between seropositive and seronegative individuals. A mean of 7.39 leucocytes × 109/L (range 2.59–17.98 × 109/L) was found, with the seropositive group presenting higher values, with a mean difference of −0.32 × 109/L compared with the seronegative individuals (Table 2). A mean proportion of 4.5% eosinophils was found, with seropositive individuals presenting significantly higher proportions of eosinophils (5.9%) compared with seronegative individuals (4.2%) (reference values: 1–4%, 0.06–0.5 × 109/L). The mean difference in absolute eosinophil counts between seropositive and seronegative individuals was also significantly different.

Socioepidemiological data The relation between seropositivity and socio-economic conditions, housing characteristics, water and excreta disposal are summarised in Table 3. With respect to socio-economic status, strata III (middle class) and IV (relative poverty) predominated, incorporating 85.7% (222/259) of the participants, with a smaller proportion of participants coming from strata II (upper middle class) and V (critical poverty), without a significant association with seropositivity. Variables such as type of housing; floor type; excreta disposal; water distribution, storage and treatment; and garbage collection showed no association with seropositivity to Toxocara spp. (Table 3). In this study, 58.3% (151/259) of the population kept a dog in their home, with 58.9% (89/151) reporting taking the dog to the veterinarian and 89.4% (135/151) reporting that their dog had been treated for worms (in the last year). The majority of the population in this study (92.7% [140/151]) reported that dogs defecated in the house, yard and garden. Likewise, 84.6% (219/ 259) reported the presence of dogs around the house and 27.8% (72/259) in recreation sites. They also stated that 53.3% (138/259) of the children had contact with the dogs and 48.7% (126/259) played with them. These two variables showed a statistically significant association with seropositivity (OR 2.3 [95% CI 1.0 to 4.9], p=0.028 and OR 2.2 [95% CI 1.0 to 4.4], p=0.036, respectively). Related variables of ownership and contact with cats showed no association with seropositivity to Toxocara spp. (Table 4). Variables such as geophagia, onychophagia and hand washing were reported but showed no association with seropositivity to Toxocara spp., while playing with soil showed a strong association (OR 3.0 [95% CI 1.4 to 6.3], p=0.003) (Table 4).

Discussion Toxocariasis can cause serious health problems in the paediatric population, affecting multiple organs in infected individuals; however, it remains one of the most neglected parasitic diseases.6,7,22 The techniques used in immunodiagnosis generally have limitations due to low specificity. The ELISA technique employed in this study was evaluated in previous reports,17,20 showing diagnostic indexes suitable for immunodiagnosis of human toxocariasis. The seroprevalence of toxocariasis found in our study was similar to or higher than that reported in some work23,24 and in most cases was lower than the results observed in other


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Table 3. Socio-economic strata, housing characteristics, water and garbage disposal and the association with the presence of anti-Toxocara spp. antibodies in studied children from two municipalities of Aragua State, Venezuela Features

Total, n (%)

Antibodies anti-Toxocara spp. Positive, n (%)

Strata according Graffar Stratum II (upper middle)a Stratum III (middle) Stratum IV (relative poverty) Stratum V (critical poverty) Type of housing Housea Apartment Makeshift dwellings Floor type, interior Ceramics/cementa Earth Floor type, exterior Ceramics/cementa Earth Excreta disposal Bathrooms sewer Sewer/environment Water distribution Intradomicilliarya Peridomiciliary Public pump Well Tanker truck Water storage Tanka Casks Bucket Others Drinking water treatment Boileda Filtered Bottle Jet (untreated) Garbage collection Common dump Urban sanitation Burned/other a

Negative, n (%)

p-Value OR (95% CI)

36 (13.9) 112 (43.2) 110 (42.5) 1 (0.4)

4 (10.8) 16 (43.2) 17 (46.0) 0 (0.0)

32 (14.4) 96 (43.2) 93 (41.9) 1 (0.45)

1.0 (–) 1.3 (0.4 to 4.2) 1.4 (0.4 to 4.6) –b

– 0.629 0.521 –

209 (80.7) 25 (9.7) 25 (9.7)

33 (89.2) 1 (2.7) 3 (8.1)

176 (79.3) 24 (10.8) 22 (9.9)

1.0 (–) 0.2 (0.0 to 1.6) 0.7 (0.2 to 2.5)

– 0.147 0.621

253 (97.7) 6 (2.3)

36 (14.2) 1 (16.7)

217 (85.8) 5 (83.3)

1.0 (–) 1.2 (0.1 to 10.6)

– 0.866

166 (64.1) 93 (35.9)

23 (13.9) 14 (15.0)

143 (86.1) 79 (85.0)

1.0 (–) 1.1 (0.5 to 2.2)

– 0.792

231 (89.2) 28 (10.8)

34 (91.9) 3 (8.1)

197 (88.7) 25 (11.3)

1.0 (–) 0.6 (0.1 to 2.4)

– 0.569

204 (78.8) 9 (3.5) 13 (5.0) 30 (11.6) 3 (1.1)

29 (78.4) 2 (5.4) 3 (8.1) 3 (8.1) 0 (0)

175 (78.8) 7 (3.2) 10 (4.5) 27 (12.2) 3 (1.4)

1.0 (–) 1.7 (0.3 to 8.7) 1.8 (0.4 to 6.9) 0.6 (0.1 to 2.3) –b

– 0.510 0.388 0.533 –

139 (64.4) 61 (28.2) 14 (6.5) 2 (0.9)

19 (61.3) 8 (25.8) 3 (9.7) 1 (3.2)

120 (64.9) 53 (28.7) 11 (6.0) 1 (0.5)

1.0 (–) 0.9 (0.3 to 2.3) 1.7 (0.4 to 6.7) 6.3 (0.3 to 105.2)

– 0.916 0.435 0.199

28 (10.8) 43 (16.6) 138 (53.3) 49 (18.9)

6(16.2) 4(10.8) 17 (46.0) 10 (27.0)

22 (9.9) 39 (17.6) 121 (54.5) 39 (17.6)

1.0 (–) 0.3 (0.1 to 1.4) 0.5 (0.1 to 1.4) 0.9 (0.3 to 2.9)

– 0.161 0.209 0.915

20 (7.7) 232 (89.6) 7 (2.7)

3 (8.1) 34 (91.9) 0 (0)

17 (7.7) 198 (89.2) 7 (3.2)

1.0 (–) 0.9 (0.2√3.5) –b

– 0.967 _

Reference category. bUncalculated.

countries,25–38 where the reported seroprevalence was between 7.7% and 86.8%, showing the cosmopolitan nature of toxocariasis. In relation to Venezuela, the seroprevalence of this study was similar to that in a study in Delta Amacuro State13 and higher than that obtained in a work in Zulia State,16 but in some cases was lower than that recorded in other studies in children,14,15 where the reported seroprevalence was between 29.5% and 58.9%. It is possible that there are more risk factors


and the rate of transmission of infection was higher in these communities or the diagnostic test or antigens employed could have had a lower specificity and the prevalence was sobrestimate by cross-reactivity with other related parasites, since the prevalence obtained in several similar studies seems to be extremely high compared with the results of the present study. When the seroprevalence of toxocariasis was compared by age group, no differences were evident, and these results are


Table 4. Pet ownership, eating habits, hygiene measures and their association with the presence of antibodies anti-Toxocara spp. in studied children from two municipalities of Aragua State, Venezuela Features

Regarding the dog Dog ownership Veterinary consultation Antiparasitic treatmenta Where defecates Home/yard/gardenb Street/unknown Handles droppings (mother) Stray dogs around the house Stray dogs in recreational places Child contact with dogs Child playing with dogs Presence of dogs within the institution Regarding the cat Cats ownership Veterinary consultation Antiparasitic treatment Where defecates Home/yard/gardenb Street/unknown Handles droppings (mother) In relation to the child Plays with soil Geophagia Hands gets into the mouth Bites nails (onychophagia) Child washes hands before eating After playing with soil After playing with dogs Mother washes hands before preparing food Visit to recreational sites (parks) a

Total, n (%)

Antibodies anti-Toxocara spp. Positive, n (%)

Negative, n (%)

OR (95% CI)

p-Value

151 (58.3) 89 (58.9) 136 (90.1)

25 (67.6) 12 (48.0) 19 (76.0)

126 (56.8) 77 (61.1) 117 (92.9)

1.6 (0.8 to 3.3) 0.6 (0.2 to 1.4) 0.2 (0.1 to 0.8)

0.220 0.227 0.015

140 (92.7) 11 (7.3) 74 (49.0) 219 (84.6) 72 (27.8) 138 (53.3) 126 (48.7) 165 (63.7)

23 (92.0) 2 (8.0) 12 (48.0) 35 (94.6) 11 (57.9) 26 (70.3) 24 (64.9) 27 (73.0)

117 (92.9) 9 (7.1) 62(49.2) 184 (82.9) 61 (50.4) 112 (50.5) 102 (46.0) 138 (62.2)

1.0 (–) 1.1 (0.1 to 6.0) 1.0 (0.4 to 2.2) 3.6 (0.8 to 15.7) 1.3 (0.5 to 3.5) 2.3 (1.1 to 4.9) 2.2 (1.1 to 4.5) 1.6 (0.8 to 3.6)

– 1.000d 0.912 0.086 0.545 0.028 0.036 0.209

62 (23.9) 8 (12.9) 17 (27.4)

13 (35.1) 1 (7.7) 1 (7.7)

49 (22.1) 7 (14.3) 16 (32.7)

1.9 (0.9 to 4.0) 0.5 (0.0 to 4.6) 0.2 (0.0 to 1.4)

0.088 1.000d 0.090d

50 (80.7) 12 (19.4) 7 (11.3)

11 (84.6) 2 (15.4) 1 (7.7)

39 (79.6) 10 (20.4) 6 (12.2)

1.0 (–) 0.7 (0.1 to 4.2) 0.6 (0.0 to 5.8)

– 1.000d 1.000d

115 (44.4) 4 (1.54) 130 (50.2) 101 (39.0) 227 (87.6) 100 (87.0) 88 (69.8) 259 (100) 140 (54.1)

25 (67.6) 1 (2.7) 22 (59.5) 14 (37.8) 31 (83.8) 20 (80.0) 15 (62.5) 37 (100) 19 (51.4)

90 (40.5) 3 (1.4) 108 (48.7) 87 (39.2) 196 (88.3) 80 (88.9) 73 (71.6) 222 (100) 121 (54.5)

3.1 (1.5 to 6.4) 2.0 (0.0 to 26.0) 1.5 (0.8 to 3.1) 0.9 (0.5 to 1.9) 0.7 (0.3 to 1.8) 0.5 (0.2 to 1.6) 0.7 (0.3 to 1.7) –c 0.9 (0.4 to 1.8)

0.003 0.462d 0.226 0.876 0.443 0.250 0.386 – 0.722

Antiparasitic treatment in the last year. bReference category. cUncalculated. dFisher’s exact two-tailed test.

similar to those of other studies.25–27 This is in contrast to reports from other studies where the highest prevalence was in the oldest groups.28–30 These results could be due to prolonged exposure to sources of infection. Nevertheless, in the previous study made in preschool children (1–6 y old) by our group,17 the seroprevalence was higher in children