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Zoonotic foci of
Toxocara
sp.: in state of Sucre, Venezuela
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º
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Neotropical Helminthology
Neotropical Helminthology, 2024, vol. 18 (2), 225-239
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
ZOONOTIC FOCI OF
TOXOCARA
SP.: COMPARISON OF TWO TOURIST
REGIONS IN THE STATE OF SUCRE, VENEZUELA
FOCOS ZOONÓTICOS DE
TOXOCARA
SP.: COMPARACIÓN DE DOS
REGIONES TURÍSTICAS EN EL ESTADO SUCRE, VENEZUELA
Erika Gomez-Martinez
1,2
, Márcia Viviana Gonçalves-Vallejos
1
, María Betania Bravo- Rodríguez
1
,
Marcos Tulio-Díaz
2
, Zulay Simoni-González
2
, Del Valle Guilarte
2
, Elizangela Farias-da Silva
2
,
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20242181825
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
Toxocariasis is a human infection caused by the larvae of the nematodes
Toxocara canis
(Werner, 1782) or
Toxocara
cati
(Schrank, 1788), which are parasitic in animals and represents a serious public health problem. T e objective of
this study was to investigate the information and prevalence of parasitic toxocariasis in the state of Sucre, Venezuela,
particularly in the municipalities of Montes and Sucre, in communities considered vulnerable due to social and
Zeca Manuel-Salimo
1,1
, Luziana de Sousa-Xavier
5
, Grafe Oliveira-Pontes
5
1
Programa de Pós-Graduação em Medicina Tropical, Universidade do Estado do Amazonas, Av. Pedro Teixeira, s/n, Dom
Pedro, 69040-000 Manaus-AM, Brasil.
2
Instituto de Investigaciones em Biomedicina y Ciencias Aplicadas Dra. Susan Tai, Universidad de Oriente IIBCAUDO. Av.
Universidad, CEP: 6101 Cumaná-Sucre, Venezuela.
3
Centro de Estudos Superiores de Tabatinga, Universidade do Estado do Amazonas, Av. da Amizade, 74 - Centro, CEP
69640-000, Tabatinga – AM, Brasil.
4
Faculdade de Ciências de Saúde, Universidade Lúrio, Nampula 364, CEP: 3100 Moçambique.
5
Fundação de Medicina Tropical Doutor. Heitor Vieira Dourado, Av. Pedro Teixeira, s/n, Dom Pedro, 69040-000, Manaus-
-AM, Brasil.
* Corresponding author: grafeoliveira@gmail.com
Er
ika Gomez-Martinez:
https://orcid.org/0000-0002-2467-8831
Márcia Viviana Gonçalves-Vallejos:
https://orcid.org/0000-0003-0657-4120
María Betania Bravo-Rodríguez:
https://orcid.org/0009-0005-2368-362X
Marcos Tulio-Díaz:
https://orcid.org/0009-0007-6392-3004
Zulay Simoni-Gonzalez:
https://orcid.org/0000-0002-5237-8238
Del Valle Guilarte:
https://orcid.org/0009-0006-3000-2463
Elizangela Farias da-Silva:
https://orcid.org/0000-0002-3386-6842
Zeca Manuel-Salimo:
https://orcid.org/0000-0002-0834-8728
Luziana de Sousa-Xavier:
https://orcid.org/0009-0000-6515-691X
Grafe Oliveira Pontes:
https://orcid.org/0000-0003-0755-1086
226
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et al.
economic defciencies within the epidemiological/sanitary monitoring. In these municipalities, many stray dogs are
living near homes and maintaining contact with other domestic dogs. Te seroprevalence of
T. canis
was evaluated
through the ELISA method. A seroprevalence of IgG anti-
T. canis
was obtained in the parish of San Juan of 90.12% and
the parish of Cumanacoa of 82.14%. In the parish of San Juan, when evaluating the prevalence of parasites by species,
T. canis
was present in 18.37% of the feces of the canines evaluated. On the other hand, in the parish of Cumanacoa,
T.
canis
was present in 9.90% of the canine samples analyzed; similarly, the presence of
Toxocara
sp. in soils in both parishes.
In summary, the determination of two zoonotic foci of
Toxocara
sp. in the state of Sucre, Venezuela, since all the factors
necessary for the transmission of toxocariasis are present.
Keywords
:
Dogs – Epidemiology – Larva migrans – Parasitic disease –
Toxocara canis
– Zoonosis
RESUMEN
La toxocariasis es una infección humana causada por las larvas de los nematodos
Toxocara canis
(Werner, 1782) o
Toxocara
cati
(Schrank, 1788), que son parásitos en los animales, y representa un grave problema de salud pública. El objetivo
de este trabajo fue investigar la información y prevalencia de toxocariasis parasitaria en el estado Sucre, Venezuela,
particularmente en los municipios de Montes y Sucre, en comunidades consideradas vulnerables por defciencias sociales
y económicas en el monitoreo epidemiológico/sanitario. En estos municipios hay muchos perros callejeros que viven
cerca de las casas y mantienen contacto con otros perros domésticos. La seroprevalencia de
T. canis
se evaluó mediante
el método ELISA. Se obtuvo una seroprevalencia de IgG anti-
T. canis
en la parroquia San Juan de 90,12% y en la
parroquia Cumanacoa de 82,14%. En la parroquia San Juan, al evaluar la prevalencia de parásitos por especie,
T. canis
estuvo presente en el 18,37% de las heces de los caninos evaluados. Por otra parte, en la parroquia Cumanacoa,
T. canis
estuvo presente en el 9,90% de las muestras caninas analizadas; Asimismo, la presencia de
Toxocara
sp. en suelos de ambas
parroquias. En resumen, la determinación de dos focos zoonóticos de
Toxocara
sp. en el estado Sucre, Venezuela, ya que
están presentes todos los factores necesarios para la transmisión de la toxocariasis.
Palabras clave:
Epidemiología – Enfermedad parasitaria – Larva migrans – Perros –
Toxocara canis
– Zoonosis
INTRODUCTION
Toxocariasis is a human infection caused by the larvae of the
nematodes
Toxocara canis
(Werner, 1782) or
Toxocara cati
(Schrank, 1788), which are parasitic in animals. Te clinical
manifestations of the disease are usually asymptomatic,
which contributes to the disease being neglected. And
yet, toxocariasis has been shown to be especially prevalent
among children from socioeconomically disadvantaged
populations, both in the tropics and subtropics and in
industrialized nations (Macpherson, 2013; Rostami
et al.,
2019; Ma
et al.,
2020).
In humans, the infection is acquired accidentally, as there is
no normal development of the parasite in humans, only the
larval stage survives as it is a paratenic host in this parasitosis
(Taylor
et al
., 2017). Infection occurs by ingestion of
infective eggs found in poorly washed vegetables and fruit
originating from a contaminated environment, geophagy,
ingestion of undercooked paratenic hosts (chicken, beef
or lamb), putting contaminated objects in the mouth, as
well as not washing hands after playing with or petting
infected dogs (Holland
et al.,
1995; Vázquez
et al.,
1997;
Ulloque-Badaracco
et al.,
2023). Children are the most
infected due to their poor hygienic habits and are often
in contact with dogs and puppies, as well as exposed to
the pets’ living environment (Cabral-Monica
et al.,
2022).
Toxocariasis is a widely distributed zoonosis, in which the
human need to keep pets and companion animals such as
dogs and cats around ensures the persistence of the parasite
and infection in humans over time. with rates ranging from
1% in Spain to 86% in Santa Lucia; from 3.6% to 24.7%
in Brazil; 47.5% in Colombia; from 34.9% to 66.6%
in Venezuela and from 37.9% (Roldán
et al.,
2010a). In
Argentina, a study carried out in children showed a 67.7%
seroprevalence of anti-
Toxocara
IgG antibodies (López
et
al.,
2005), while in Paraguay a 78% seroprevalence for
toxokaryosis was reported (Rivarola
et al.,
2009). In Peru,
a few reports have informed of frequencies from 7.8% to
44.92% in rural populations from diferent places (Roldán
et al.,
2010a).
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Toxocara canis
infection in dogs has worldwide
distribution rates ranging from 0 to 99.4% (Barriga,
1988; Heymann & American Public Health Association,
2004; Borges & Ferreira, 2020). In Venezuela, studies on
T. canis
infection were carried out in urban areas such
as Caracas, reporting prevalences of 66.6%, in rural and
suburban communities of the Capital District and the
State of Miranda 20% and 70% (Incani, 1996; Delgado
& Rodríguez-Morales, 2009). In the Brazilian Amazon,
the prevalence in urban children < 5 years of age has been
reported to be 21.5%,increasing to 26.7% in the rural
general population, and to 26.8%or 52% in the riverine
population (Oliart-Guzmán
et al.,
2014). Furthermore,
studies on canine toxocariasis carried out in Maracaibo
reported a prevalence of 11.4% (Ramírez-Barrios
et al.,
2004) and 63,16% in soil samples from leisure parks
(Cazorla-Perfetti
et al.,
2007). In eastern Venezuela,
particularly in the state of Anzoátegui, (Fernández
et
al.,
2009) carried out a study on children aged 6 to 8
years, obtaining a prevalence of 16%, and (Gómez, 2004)
carried out a study in the Nueva Toledo neighborhood of
El Peñón, state of Sucre, on children aged 2 to 15 years,
with prevalences of 77.14%.
T us, the present study evaluated the seroprevalence of
toxocariasis in the municipalities of Montes and Sucre,
which are regional tourist destinations in Venezuela. T ese
regions were selected to be considered vulnerable due to
social and economic deprivation, the large number of
stray dogs found in the area, and the fact that most family
groups have dogs as pets.
MATERIAL AND METHODS
Study area
T e present study was conducted in the municipalities of
Sucre and Montes, in the state of Sucre, Venezuela (Fig.
1). T e municipality of Sucre is located in a mountainous
area with a hot, semi-arid climate, with average
temperatures of 27°C and 440 mm of precipitation with
a rainy season from July to November (Pérez, 2006).
T e second site was Cumanacoa in the municipality of
Montes. It is characterized by a hot sub-humid climate
with temperatures ranging from 21°C to 27°C and annual
precipitation between 900 and 1500 mm.
Figure 1
. Map of the state of Sucre, Venezuela with the respective municipalities evaluated: Sucre (10,24198° N, 64,27980°
O), Cumanacoa (10,24720° N, 63,92019° O), Google Maps.
Population sample
To calculate the representative sample size, a formula
proposed by Martínez (2003) for f nite populations, with
a known sampling frame, was used. T e prevalence for
toxocariosis of 74.14% was considered (Gómez, 2004). In
the parish of San Juan, 172 blood and faeces samples were
taken from people who voluntarily attended the survey.
T e same occurred in the parish of Cumanacoa, where
100 blood and stool samples were taken, respectively. A
clinical-epidemiological survey was administered to each
individual, regardless of gender and age, in each parish,
with prior informed consent (OPAS, 1993).
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Human faecal samples
All the people who atended and participated in the collection
were asked to provide a stool sample for the evaluation
of the diferent helminths including
Ascaris lumbricoides
(Linnaeus, 1758). As an ascaridium,
A. lumbricoides
cross-
reacts with
T. canis
when using immunological techniques
using sera to evaluate for anti-
T. canis
antibodies. Serum
samples of individuals presenting with
Ascaris lumbricoides
eggs in their stool was excluded from the study.
Human blood samples
Blood samples were obtained from the participants by
venous puncture and transferred to the parasitology
laboratory at the Instituto de Investigaciones en
Biomedicina y Ciencias Aplicadas “Dr. Susan Tai”,
Universidad de Oriente (IIBCA-UDO), Venezuela, where
they were processed for serum collection. Te collected
sera were frozen at -20°C until analysis.
Determination of anti-T
. canis
IgG antibodies by
ELISA method
A commercial
Toxocara
-IgG ELISA kit (RIDASCREEN
Toxocara
-IgG), which uses excretion-secretion antigens,
was used for serological diagnosis. No absorption of sera
with
Ascaris suum
(Goeze, 1782) antigen was performed.
However, all individuals with
A. suum
eggs in their faeces
were excluded from analysis. For the evaluation and
interpretation of the results, the sample was considered
as positive for anti-
T. canis
antibodies when its index was
higher than 1.10, as a negative sample, that with an index
lower than 0.90 and as an indeterminate sample that with
an index between 0.90 – 1.10 (Fernández
et al.,
2009).
Dog Fecal Samples
In both parishes, with the consent of the owners the dog
fecal samples were collected in the morning, at midday
and in the afternoon, and placed in airtight containers and
transported to the laboratory. If not analyzed on the day of
collection, they were stored at 4°C.
Soil samples
Soil samples were collected from the courtyards of homes
in communities from the San Juan and Cumanacoa
parishes. Tese samples were obtained by superfcially
scraping the courtyards with a spatula, 5 cm from any
faecal matter after a random selection of sites with bare
soil. Soil samples were collected upto 10 cm deep and
stored in labeled polyethylene bags at room temperature
until processing (Leventhal & Cheadle, 1992).
Parasitological diagnosis
Small portions of all the stool samples were examined
by direct microscopic examination after mixing with
0.85% physiological saline and Lugol’s solution (Botero
& Restrepo, 1998). In addition, concentration and
enrichment techniques such as: spontaneous tube
sedimentation and fotation by Willis-Malloy were applied
(Quinn
et al.,
1980; Camacho
et al.,
2006). It was also
carried out with soil samples taken in each parish. Tese
examinations were also done on soil samples taken in each
parish.
Statistical analysis
Te results obtained were expressed as percentages and
represented in tables and graphs. Te seroprevalence of
T.
canis
infection was determined by applying the formula
described by Gordis (2004). Te Chi-square test (
χ
²) was
used to establish the association between the clinical-
epidemiological aspects evaluated and the seroprevalence
of
T. canis
in the inhabitants of San Juan and Cumanacoa
parishes (Martínez, 2003). Data was analyzed using SPSS
18 software.
Ethics aspects:
Tis research was approved by the
IIBCAUDO Bioethics and Biosafety Committee,
(CBBIIBCAUDO-2009-09-3) year 2009, September,
project 3.
RESULTS
The seroprevalence of
T. canis
was evaluated using
the
Toxocara
IgG commercial kit. Of the 172 serum
samples analyzed from the parish of San Juan, 10
samples were discarded because they belonged to
people who had
A. lumbricoides
eggs in their faeces. Of
the remaining 162 sera, 146 (90.12%) were positive,
9 (5.56%) indeterminate and 7 (4.32%) negatives.
The average sample index of the positive cases was
3.03 of the indeterminate 0.99 and of the negative
0.55 (table 1). From the 100 serum samples analyzed
from the Cumanacoa parish, Montes municipality, 16
sera were discarded because they belonged to people who
had
A. lumbricoides
eggs in their stool samples. Of the 84
remaining sera, 69 (82.14%) were positive, 6 (7.14%)
indeterminate and 9 (10.17%) negatives, the average
sample rate for positive cases was 2.18, for indeterminate
cases 0.96 and for negative cases 0.60 (table 1).
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Table 1
. Seroprevalence and summary statistics of sample rates for IgG anti-
T. canis
antibodies in inhabitases of San Juan
and Cumanacoa (Sucre and Montes municipality), Sucre state, Venezuela.
Inhabitants of San Juan / Cumanacoa
Samplesn.%
χ
SDLLUL
Positive146/6990,12/82,143,03/2,181,22/0,941,20/1,137,74/5,04
Indeterminate9/65,56/7,140,99/0,960,08/0,040,91/0,921,10/1,02
Negative7/94,32/10,170,55/0,600,14/0,210,37/0,340,73/0,89
n: number of cases,
χ
: mean, SD: standard deviation, LL: lower limit, UL: upper bound %: percentage.
To understand the epidemiology of toxocariasis in both
parishes of Sucre municipality, Sucre state, Venezuela, the
seroprevalence of anti-
T. canis
IgG was analyzed according
to gender; it was found that females were more afected
in both San Juan and Cumanacoa parishes. However,
the chi-square test did not show a statistically signifcant
association (table 2).
Table 2
. Association between genders of inhabitants and seroprevalence of anti-
Toxocara canis
IgG in San Juan and
Cumanacoa (Sucre and Montes municipality), Sucre state, Venezuela.
IgG Anti-Toxocara canis in Inhabitants of San Juan / Cumanacoa
PositivesIndeterminateNegativesTotal
Gendern%n%n%n%
Females102/4569.86/65,227/377.80/502/628.57/66.67111/5468.52/,64.29
Males44/2430.14/34,782/322.20/505/371.43/33.3351/3031.48/35.71
Total 146/69100/1009/6100/1007/9100/100162/84100/100
χ
2
= 5,66 ns p= 0,06 /
χ
2
= 0,58 ns p= 0,75
n: number of cases %: percentage
χ
2: chi-square ns: not signifcant p: probabilit
y
Table 3 show the seroprevalence of anti-
T. canis
IgG and
its distribution according to age group, with signifcant
results in the Cumanacoa and San Juan parishes where the
0-10 age group was the most afected. Curiously, the chi-
square test showed no signifcant association within this
age group from the San Juan parish, which was also the
most afected.
Table 3
. Association between age and seroprevalence of anti-Toxocara canis IgG in inhabitants of San Juan and Cumanacoa
(Sucre and Montes municipality), Sucre state, Venezuela.
IgG Anti-Toxocara canis in Inhabitants of San Juan / Cumanacoa
PositivesIndeterminateNegativesTotal
Age (years)n%n%n%n%
0-10 55/3837,67/55,075/455,56/66,676/485,71/44,44 66/4640,74/54,76
11-20 31/1321,23/18,841/011,11/00/0 0/0 32/1319,75/15,48
21-30 21/914,38/13,041/011,11/00/3 0/33,33 22/1213,59/14,29
31-40 13/1 8,90/1,450/0 0/01/114,29/11,11 14/2 8,64/2,38
41-50 4/1 2,74/1,450/2 0/33,330/1 0/11,11 4/4 2,47/4,76
51-60 11/4 7,53/5,802/022,22/00/0 0/0 13/4 8,02/4,76
61-70 7/3 4,80/4,350/0 0/00/0 0/0 7/3 4,32/3,57
(Continúa Tabla 3)
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71-80 3/0 2,05/00 0/00/0 0/0 3/0 1,85/0
81-90 1/0 0,70/00 0/00/0 0/0 1/0 0,62/0
Total146/69 100/1009/6 100/1007/9 100/100162/84 100/100
χ
2
= 12.80 ns p= 0.69
n: number of cases %: percentage
χ
2: chi-square ns: not signifcant *s: signifcant p: probability
T
able 4 show the seroprevalence of anti-
T. canis
IgG
and its distribution according to handwashing practices
before eating, food preparations and contact with soil by
individuals in both parishes. Tere was no statistically
signifcant association with any of the variables assessed by
the chi-square test. Tis was contrary to the self-declared
food handling and handwashing practices. Majority of
those testing positive for anti-
T. canis
IgG antibodies
individuals declared washing their hands before eating
(84.93% San Juan parish) and (92.75% Cumanacoa
parish) or cleaning their food together with handwashing
before consumptio (75.34% for San Juan parish, and
85.51% for Cumanacoa parish). We also disclose that at
the time of the surveys many of the people, particularly
children, had dirty fngernails. In addition, if they washed
their hands or wash their food (fruits and vegetables),
they did so using water from the rivers that transversed
these parishes. Te water used was neither treated nor
boiled, further compounding to the environmental
contamination of these uncooked foodstufs with
T. canis
eggs and other parasites. Te results from both parishes
were comparable.
Table 4
. Association between hand washing practices before eating, foodstuf handling parctices, contact with soil and
seroprevalence of anti-Toxocara canis IgG in inhabitants of San Juan and Cumanacoa (Sucre and Montes municipality),
Sucre state, Venezuela
IgG ANTI-Toxocara canis in Inhabitants of San Juan / Cumanacoa
PositivesIndeterminateNegativesTotal
n%n%n%n%
Hand washing before eating
Yes124/6484,93/92,757/577,78/83,337/8100/88,89138/7785,19/91,67
No22/515,07/71,252/122,22/16,670/10/11,1124/714,81/8,33
Total146/69100/1009/6100/1007/9100/100162/84100/100
χ
2
= 1,62 ns p= 0,44 /
χ
2
= 0,74 ns p= 0,69
Foodstuf washing and
cleaning
Yes110/5975,34/85,517/477,78/66,675/771,43/77,78122/7075,31/83,33
No36/1024,66/14,492/222,22/66,672/228,57/22,2240/1424,69/16,67
Total146/69100/1009/6100/1007/9100/100162/84100/100
χ
2
= 0,09 ns p= 0,96 /
χ
2
= 1,63 ns p= 0,44
Contact with soil
Yes92/4763,01/68,127/377,78/506/485,71/44,44105/5464,81/64,29
No54/2236,99/31,882/322,22/501/514,29/55,5657/3035,19/35,71
Total146/69100/1009/6100/1007/9100/100162/84100/100
χ
2
= 2,21 ns p= 0,33 /
χ
2
= 2,52 ns p= 0,28
n: number of cases %: percentage
χ
2: chi-square ns: not signifcant p: probability
An analysis of anti-
T. canis
IgG seroprevalences and their
distribution with regard to presence and contact with dogs
by the participants from the two parishes is shown in table
5. Te sero-conversion status was not associated with the
contact with dogs.
(Continúa Tabla 3)
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Table 5
. Association between the presence of dogs, contact with dogs and the seroprevalence of anti-
Toxocara canis
IgG in
inhabitants of San Juan and Cumanacoa (Sucre and Montes municipality), Sucre state, Venezuela.
IgG ANTI-Toxocara canis in Inhabitants of San Juan / Cumanacoa
PositivesIndeterminateNegativesTotal
n%n%n%n%
Dog present
Yes99/2367,81/33,338/366,89/504/657,14/66,67111/3268,52/38,10
No47/4632,19/66,671/311,11/503/342,86/33,3351/5231,48/61,90
Total146/69100/1009/6100/1007/9100/100162/84100/100
χ
2
= 2,19 ns p= 0,33 /
χ
2
= 4,14 ns p= 0,13
Contact with
dogs
Yes60/4841,10/69,577/677,78/1003/442,86/44,4470/5843,20/69,04
No86/2158,90/30,432/022,22/04/557,14/55,5692/2656,80/30,96
Total146/69100/1009/6100/1007/9100/100162/84100/100
χ
2
= 4,659 ns p= 0,09 /
χ
2
= 5,25 ns p= 0,07
n: number of cases %: percentage
χ
2: chi-square ns: not signifcant p: probability
Tese tables show the seroprevalence of anti-
T. canis
IgG
and its distribution according to age, deworming and time
of deworming of pet dogs of the participants from in both
parishes. However, there were no signifcant associations
established (Table 6).
Table 6
. Role of age, deworming status, and time of deworming of pet dogs in the anti-Toxocara canis IgG seroprevalence
of inhabitants of San Juan and Cumanacoa (Sucre and Montes municipality), Sucre state, Venezuela.
IgG ANTI-Toxocara canis in Inhabitants of San Juan / Cumanacoa
VariablesPositivesIndeterminateNegativesTotal
n%n%n%n%
Age of dog
6 months-1 year41/1341,41/56,524/050/04/3100/5049/1644,14/50
Older than 1 year58/1058,59/43,484/350/1000/30/5062/1655,86/50
Total99/23100/1008/3100/1004/6100/100111/32100/100
χ
2
= 5,47 ns p= 0,06 /
χ
2
= 3,39 ns p= 0,18
Received dewormer
Yes39/1439,40/60,873/237,60/33,331/525/83,3343/2138,74/65,63
No60/960.60/39,135/162,50/66,673/175/16,6768/1161,26/34,37
Total99/23100/1008/3100/1004/6100/100111/32100/100
χ
2
= 0,34 ns p= 0,84 /
χ
2
= 1,07 ns p= 0,59
Deworming time
At birth10/010,10/01/012,50/00/00/011/09,91/0
Monthly11/011,11/00/00/00/00/011/09,91/0
Every 6 months11/611,11/26,091/012,50/01/325/5013/911,71/28,13
Annually7/87,07/34,781/212,50/33,330/20/33,338/127,21/37,50
Never60/960,61/39,135/162,50/66,673/175/16,6768/1161,26/34,37
Total99/23100/1008/3100/1004/6100/100111/32100/100
χ
2
= 3,16 ns p= 0,92 /
χ
2
= 3,35 ns p= 0,50
n: number of cases %: percentage
χ
2: chi-square ns: not signifcant p: probability
232
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Gomez-Martinez
et al.
It was observed that puppy owners do not provide
adequate deworming treatment, of which after 3- or
4-weeks puppies begin to shed
T. canis
eggs freely into the
soil, where they become infective. Consulted databases did
not produce any published work on this parasitosis that
considered these epidemiological variables. Both parishes
had diferent patterns of behavior in relation to these
items, but no statistically signifcant association was found
in either parish.
Tere was a statistically signifcant association with the
collection of canine faeces by their owners in the parish
of Cumanacoa, where 91.30% of the animals defecated
in the yard and 78.26% of the owners did not collect the
dog fecal matter. Tus, these faeces, together with the
evolutionary forms of parasites in the contaminated fecal
material can develop and be ready for infection (Table 7).
Table 7
. Association between location of dog defecation, collection of dog faeces by dog owners, the frequency of dog faeces
collection and disposal, and the seroprevalence of anti-
Toxocara canis
IgG in inhabitants of San Juan and Cumanacoa (Sucre
and Montes municipality), Sucre state, Venezuela.
IgG ANTI-Toxocara canis in Inhabitants of San Juan / Cumanacoa
VariablesPositivesIndeterminateNegativesTotal
n%n%n%n%
Location of dog
defecation
Courtyard81/2181,82/91,307/287,50/66,674/5100/83,3392/2882,88/87,50
Ticket17/017,17/00/00/00/00/17/015,32/0
House1/21,01/8,701/112,50/33,330/10/16,672/41,80/12,50
Total99/23100/1008/3100/1004/6100/100111/32100/100
χ
2
= 7,73 ns p= 0,10 /
χ
2
= 1,59 ns p= 0,45
Collection of faeces
Yes51/551,52/21,746/175/33,334/5100/66,6761/2654,96/81,26
No48/1848,48/78,262/225/66,670/10/33,3350/645,05/18,75
Total99/23100/1008/3100/1004/6100/100111/32100/100
χ
2
= 5,05 ns p= 0,08 /
χ
2
= 8,01 ns p= 0,02
Contact with the site
Yes51/2051,52/86,966/275/66,674/4100/83,3361/1154,96/34,37
No48/348,48/13,042/125/33,330/20/16,6750/2145,05/65,63
Total99/23100/1008/3100/1004/6100/100111/32100/100
χ
2
= 5,05 ns p= 0,08 /
χ
2
= 8,01*s p= 0,02
n: number of cases %: percentage
χ
2: chi-square ns: not signifcant *s: signifcant p: probability
In summary, we have established prevalence of the
Toxocara
infection in human subjects, dogs (pets and strays) and in
soil samples obtained from the vicinity of the homes and
playgrounds. Tus, we have identifed two zoonotic foci
of potential
Toxocara
sp. transmission and maintenance
parasite life cycle in Sucre state. An epidemiological map
was charted comparing the situation in Sucre state with
other states in Venezuela (Fig. 2).
233
Zoonotic foci of
Toxocara
sp.: in state of Sucre, Venezuela
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Figure 2
. Prevalence of
Toxocara
sp. in Sucre state compared to states in Venezuela with existing reports of
Toxocara
sp.
studies.
DISCUSSION
Te parish of San Juan, Sucre municipality, Sucre state,
Venezuela, is a rural area dedicated to agriculture and
animal husbandry (pigs, cattle, and poultry) usage.
Tese activities are both a source of income and food, as
well as an area of regional tourism. Te municipality of
Montes carries out similar economic activities, especially
agriculture and livestock farming with a special emphasis
on sugar cane, cofee, vegetable crop production and cattle,
poultry and pig rearing.
We found high seroprevalence of
T. canis
(Table 1),
nonetheless, globally, the prevalences reported are lower
than those of this study: in Colombia, a prevalence of
39% was reported, in Argentina 37% and in Brazil 28%
(Ulloque-Badaracco
et al.,
2023). However, a study in
Paraguay (78%), but not in Turkey (7.6%) and Italy
(31.87%) reports prevalences similar to those obtained in
this study (Rivarola
et al
., 2009; Akdemir, 2010; Qualizza
et al
., 2011).
In Venezuela, most studies on
T. canis
infection in humans
have been carried out in the central north, west and south
of the country. In Amazonas, a seroprevalence of 19.66%
was found (Oliart-Guzmán
et al.
, 2014), in preschool
children in Aragua state, Venezuela, were detected in 29%
(65/224) of children. Te seroprevalence in the diferent
preschools studied ranged between 4.2% and 60.6%
(Martínez
et al.,
2015). In Zulia state, García
et al.
(2004)
found a prevalence of 9.72% while a study conducted in
Barquisimeto, a seroprevalence of 44.60% was reported
(Delgado
et al
., 2009).
Few studies have been conducted on
T. canis
infection
in eastern Venezuela. Gómez (2004), for instance,
obtained a 77.14% prevalence in Sucre State, using the
ELISA method, while Fernández
et al.
(2009), using the
RIDASCREEN ELISA technique, reported a prevalence
of 19.0% in Anzoátegui State. It is noteworthy that
participants evaluated in this study, from both parishes,
have high prevalence rates, a refection of zoonotic foci
present in these communities.
234
Neotropical Helminthology (Lima). Vol. 18, N
º
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Gomez-Martinez
et al.
Te seroprevalence of anti-
T. canis
IgG according to
gender, was found that females were more afected in both
San Juan and Cumanacoa parishes (Table 2). Comparable
results were obtained by Espinoza
et al.
(2003) and
Gómez (2004), who found a higher seroprevalence in
females with 57.80% and 61.11%, respectively. However,
these fndings difer from those by Martín
et al.
(2008),
Delgado
et al
. (2009), Akdemir (2010) and Wisniewska
et
al.
(2011) who report that 57.63%, 51.86%, 77.80% and
62.14%, respectively, were in males. Nevertheless, Roldán
et al.
(2010b) mentioned that the gender of the individual
seems not to be an important predisposing factor for
toxocariasis in human populations.
Te results found in the age group of both municipalities
coincide with those reported by various authors such as
Aguiar-Santos
et al.
(2004) who reported a prevalence of
60% in children under 10 years of age and Gómez (2004)
who reported a prevalence of 40.74% in children aged
2-4 years. Similarly, López
et al
. (2005) reported 67.70%
in children aged 1-14 years while Fernández
et al.
(2009)
recorded a prevalence of 22.50% in children aged 6 years
and Rivarola
et al.
(2009) found a prevalence of 64.15%
in children aged 3 to 9 years. However, none of these
researchers found age-group specifc diferences in the
occurrence of toxocariasis. García
et al
. (2004) suggested
that the reduced risk of infection in older individuals
might be due to improved hygienic habits and spending
more time away from home thus distancing them from
sources of infection. It was proposed that this parasitic
infection was most likely to occur at home more than
at school or at work, where sanitary and infrastructural
conditions were better.
It is important to highlight that in the two parishes; the
schools are close to rivers and surrounded by felds, where
children carry out their recreational activities, and where
dogs defecate openly consequently depositing parasite
eggs. Additionally, many of these communities and schools
lack piped water and thus draw water from the rivers for
consumption by children and residents. Subsequently,
residents of these communities, including school children,
are exposed to contracting this parasitosis both at home
and in their schools.
Tese results difer from those obtained by Acero
et al.
(2000), who found that 46.15% of children never washed
their hands before eating and by Gómez (2004) who found
that 62.96% of the
Toxocara
seropositive children did not
wash their hands before eating, but 100% of them declared
washing their food before consumption, particularly those
to be eaten raw.
Most participants from San Juan (63,01%) and Cumanacoa
(68,12%), had contact
with T. canis
soil contaminated,
had parasitized dogs and did not wash their hands well
before eating or ingesting food. Tese participants were
predisposed to high risk of easily getting infected. Tese
rates were comparable to results found by Acero
et al.
(2000) who reported that 53.85% of toxocara-infected
children consumed soil, had poor hygiene practices, López
et al.
(2003) found that 30% of toxocariasis positive
children had a history of geophagy whilst Delgado
et al.
(2009) noted that 96.3% of the infected children had a
history of geophagy.
In both evaluated parishes, there were large tracts of land,
contaminated with canine faeces, and consequently
T. canis
eggs. At the same time, these felds served as playgrounds
for the children or fruit and vegetable gardens.
Concerning the presence of dogs in the homesteads,
67.81% of the seropositive individuals in the San Juan
parish stated that they had dogs as pets, which difered
from those of Cumanacoa parish (33.33%). However,
it should be noted that majority of the inhabitants from
both parishes declared coming in contact with other
canines in the area due to the large and uncontrolled
population of stray dogs found in both parishes. Gómez
(2004) found that 52.26% of seropositive participants had
dogs while Martín
et al.
(2008) reported that 74.57% of
those seropositive for IgG anti-
T. canis
antibodies owned
dogs. However, in a study evaluating playgrounds in
Turkey, Akdemir (2010) found that only 7.60% of those
seropositive had dogs. We note that having dogs as pets
was not signifcantly associated with testing positive for
the IgG anti-
T. canis
antibodies.
Fan
et al
. (2004) argued that toxocariasis is not related to
dog breeding, but dog breeding is a condition that in most
cases contributed to the occurrence of infection, especially
in low socio-economic societies. Similarly, Alonso
et al
.
(2004) pointed out that neither direct contact with dogs,
even puppies, nor the presence of the animals in the home
are sufcient conditions for acquiring
T. canis
infection;
other epidemiological circumstances had to coincide
to favor the risk of an infection being acquired from a
contaminated environment.
Some studies suggest that the likelihood of infection had
more to do with individual susceptibility, and behavioral
and hygienic habits rather than with the environmental
factors present in the population. Considering this, we
sought to understand if epidemiological variables such
as age of the canines present, deworming and time of
deworming of the individuals who indicated that they
owned dogs and the seroprevalence of anti-
T. canis
IgG.
235
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Neotropical Helminthology (Lima). Vol. 18, N
º
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Te majority of the seropositive individuals in the parish
of San Juan stated that their dogs defecated in the yard
(81.82%), 51.52% reported collecting dog faeces and
frequenting the place of disposal, 27.27% disposed of
these faeces in the thicket and 15.15% accumulated
them until the waste collection day. Tis was indicative
that these individuals also had frequent and direct contact
with
T. canis
contaminated dog faeces in addition to being
surrounded by animal waste subsequently increasing
the possibility of parasite transmission and reinfection.
In the databases consulted, no published studies on this
parasitosis were found that took these epidemiological
variables into account.
One of the main sources of
T. canis
infection found
within the homesteads are gardens and yards heavily
contaminated with dog faeces. Additionally, the ease with
which unwormed dogs access homes greately contributes
to this contamination and high likelihood of infection.
It is estimated that one gram of faeces from an infected
animal can harbour about 10.000
T. canis
eggs, while a
female parasite can shed up to 200.000 eggs daily into the
environment. Larval eggs can survive up to 10 years in the
environment if conditions are right, thanks to their high
resistance (García
et al
., 2004).
Taking into account the observations by García
et al
.
(2004) and Alonso
et al
. (2004), geophagia, the high dog
population, the manner in which dogs are kept without
restrictions of space or specifc places to defecate, and the
lack of collection of excrement from stray dogs, the parishes
of San Juan and Cumanacoa have become a favorable place
for the transmission of this zoonosis. In these localities,
the prevalent conditions expose the inhabitants, especially
children, to the parasite-contaminated excrement.
Te population sample studied corresponded to
individuals from two diferent socio-economic and cultural
backgrounds, but with the same social defciencies. Tis
could explain why no major diferences in risk factors
association were found between serology-positive and
serology-negative patients.
Additionally, a representative sample of canine faeces was
also taken and evaluated for parasitological contamination
in these communities. In the parish of San Juan, 93.87%
(46 of 49) of the canine faecal samples were parasitized of
which the prevalence of
T. canis
was 18.37%. Similarly, in
the parish of Cumanacoa, 65.40% (53 of 81) of the samples
were parasitized, of which 9.90% were the
T. canis
species.
Tis is indicative of which shows the risk of infection with
T, canis
in both communities. Tses fndings are similar
to those of Ramírez-Barrios
et al.
(2004) and Devera
et
al.
(2008) that showed a 11.4% and 16.7% prevalence of
canine intestinal parasites in Venezuela, specifcally in the
city of Maracaibo and Ciudad Bolívar.
In addition to the faecal samples, soil samples were also
analyzed. Of the 35 and 28 soil samples from San Juan
and Cumanacoa parishes analyzed, 5.0% and 10.71%
were positive for
Toxocara
sp. Eggs, respectively. We
however declare that at the time of soil collection, the
weather condition in the localities was unpredictable,
with constant and torrential rains, such that the parasite
eggs in the soil could have been washed by Surface run
of into the rivers that fow through the communities.
Despite the weather conditions, the presence of
Toxocara
sp. eggs in the soil of both parishes in Sucre municipality,
Sucre State, Venezuela, demonstrates the high risk of
contact and possible accidental ingestion by children in
these communities. Tis subsequently predisposes them to
acquiring the Visceral or Ocular Larva Migrans syndrome,
in addition to advancing high infection rates in dogs. Very
heterogeneous result was reported by Laiño
et al.
(2024),
(1.5%) and Antonio
et al.
(2020) (32.5%).
Comparing with other studies around Venezuela, from the
two zoonotic foci evaluated in Sucre State demonstrates
that this region has one of the highest seroprevalences
of toxocariasis in humans. However, Anzoátegui State
reports the highest prevalence of
Toxocara
sp. in canines
while Zulia State has the highest rate of soil infected with
Toxocara
sp. eggs (Cazorla-Perfetti
et al
., 2007; Tortolero
et al
., 2008; Devera
et al
., 2008; Fernández
et al
., 2009;
Nieves
et al.
, 2012; Apóstol
et al.,
2013). We are of the
opinion that the high seroprevalence is attributed to
the rural condition of both parishes evaluated in Sucre
State. It is further compounded by the lack of a Zoonosis
department in the local government to manage the large
number of stray dogs in the communities and promote
civic education on disease, dynamics of transmission,
consequences of infection.
As a zoonosis and geohelminthiasis, this parasitosis
represents a public health problem for both parishes
in Sucre State. Its epidemiology depends closely on
maintaining the chain of infected domestic and/or stray
dogs and cats, on human contact with soil contaminated
with the infected and on the general habits and attitudes
that tend to acquire the infection. It is crucial that the
public health authorities implement a control and health
education plan to raise awareness of the forms of contagion
of this parasitosis and the most appropriate way to prevent
it. Primary prevention should focus on veterinarial control
of pets, culling of stray dog populations and improving
habits and attitudes that tend to maintain the infection in
both municipalities of Sucre State, Venezuela.
236
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Gomez-Martinez
et al.
Author contributions
:
CRediT (Contributor Roles
Taxonomy)
EGM
= Erika Gomez-Martinez
MVGV
= Márcia Viviana Gonçalves-Vallejos
MBBR
= María Betania Bravo-Rodríguez
MTD
= Marcos Tulio-Díaz
ZSG
= Zulay Simoni-Gonzalez
DVG
= Del Valle Guilarte
EFS
= Elizangela Farias-da Silva
ZMS
= Zeca Manuel-Salimo
LSX
= Luziana de Sousa-Xavier
GOP
= Grafe Oliveira-Pontes
Conceptualization
: EGM, GOP, ZSG, DVG
Data curation
: GOP, LSX, ZMS
Formal Analysis
: EGM, DVG, ZSG, GOP
Funding acquisition
: EGM, GOP, LSX, MBBR, MVGV,
MTD, ZMS, ZSG, DVG, EFS
Investigation
: EGM, DVG, ZSG, MTD, MBBR, EFS
Methodology
: EGM, DVG, ZSG
Project administration
: EGM, DVG, ZSG
Resources
: EGM, DVG, ZSG
Software
: EGM, DVG, ZSG
Supervision
: EGM, ZMS, GOP
Validation
: EGM, GOP
Visualization
: EGM, GOP
Writing – original draft
: EGM, GOP, LSX, MVGV, ZMS
Writing – review & editing
: EGM, GOP, LSX, MBBR,
MVGV, MTD, ZMS, ZSG, DVG, EFS
ACKNOWLEDGMENTS
Tis work was fnanced by Instituto de Investigaciones
Cientifcas en Biomedicina y Ciencias Aplicadas, “Susan
Tai” IIBCAUDO, the Universidad de Oriente, estate
Sucre, Venezuela. Te authors would like to thank all the
participants and their families who accepted to participate
in the research and contributed to the study.
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Received October 5, 2024.
Accepted December 14, 2024.