emi00240 91..93


Original Research Paper
Low Toxocara Seroprevalence in People in Rural Durango, Mexico

Cosme Alvarado-Esquivel1*, Ángel Osvaldo Alvarado-Félix2 and Gustavo Alexis Alvarado-Félix2

1

Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State,
Avenida Universidad S/N, 34000 Durango, Mexico

2

Colegio Anglo-Español Durango, Avenida Real del Mezquital 92, 34199, Durango, Mexico

Received: 27 Jun 2019; accepted: 10 Jul 2019
*Author for c
de Medicina
México; Tel/F

DOI: 10.155

© 2019 The

This is an
(https://creat
purposes, pr
The epidemiology of Toxocara infection in rural Mexico is largely unknown. Therefore, we sought to determine
the seroprevalence of Toxocara infection in rural people in a northern Mexican state. We performed a cross-sec-
tional seroprevalence study of 641 people living in rural Durango State including 282 subjects of the general popu-
lation, 214 subjects of Huichol ethnicity, and 145 subjects of Mennonite ethnicity. Sera of participants were
analyzed for the presence of anti-Toxocara immunoglobulin G (IgG) antibodies using a commercially available en-
zyme immunoassay. Three (0.5%) of the 641 subjects tested were positive for anti-Toxocara IgG antibodies. Of the
3 Toxocara seropositive subjects, two were females, aged 19 and 39 years, and one was male, aged 59 years. They
had contacted with dogs, cleaned cat excrement, consumed unwashed raw fruits, contacted soil, or lived in a house
with soil floors. Seroprevalence of Toxocara infection was similar among the 3 groups of population studied: 0.4%
for the general population, 0.9% for Huicholes, and 0.0% for Mennonites (P = 0.41). In conclusion, the Toxocara
seroprevalence found in subjects in rural Durango is low as compared with those reported in people from rural
areas in other countries.

Keywords: cross-sectional study, epidemiology, rural, ethnic groups, seroprevalence, toxocariasis
Introduction

The parasite Toxocara is the most ubiquitous intestinal
nematode in dogs and cats [1]. This parasite is a zoonotic
pathogen that causes toxocariasis and associated complications
including allergic and neurological disorders [2]. Toxocariasis
is one of the most commonly reported zoonotic helminth in-
fections in the world [3]. Transmission to humans occurs by
accidental infection of eggs present in, for instance, contami-
nated fruits or vegetables [4]. Toxocariasis is a neglected dis-
ease reaching high prevalence independently of the economic
conditions [5]. Most human infections are asymptomatic [6].
Patients with toxocariasis may present fever, respiratory symp-
toms, gastrointestinal features [7], decreased visual acuity,
eyestrain, headache, paleness [8], paresthesias, nervousness,
and lipothymic states [9]. Ocular toxocariasis may lead to
blindness [10]. Cardiac involvement is a rare but potentially
life-threatening complication in Toxocara infection [11].

Living in rural areas is considered a risk factor for Toxocara
infection as demonstrated in studies in several countries in-
cluding Iran [12], Gabon [13], Korea [14, 15], Egypt [16],
and Poland [17]. Knowledge about the seroepidemiology of
Toxocara infection in rural Mexico is quite limited; however,
we are aware of only one study about the seroepidemiology of
Toxocara infection in rural Mexico. In a serosurvey of 126
Tepehuanos (an indigenous ethnic group) in rural Durango
State, a 26.2% seroprevalence of Toxocara infection was
found [18]. In the present study, we attempted to determine
the seroprevalence of Toxocara infection and its association
with the sociodemographic, clinical, and behavioral character-
istics of the general population in the rural communities in the
northern Mexican state of Durango.
orrespondence: Laboratorio de Investigación Biomédica, Facultad
y Nutrición, Avenida Universidad S/N, 34000 Durango, Dgo,
ax: 0052-618-8130527; E-mail: alvaradocosme@yahoo.com

6/1886.2019.00015

Author(s)

open-access article distributed under the terms of the Creativ
ivecommons.org/licenses/by-nc/4.0/), which permits unrestricted
ovided the original author and source are credited, a link to the
Materials and Methods

Study Design. We performed a cross-sectional serosurvey
using serum samples from previous Toxoplasma gondii
seroepidemiology studies [19–21]. The aims of the original
studies were to determine the seroprevalence of and risk
factors for Toxoplasma gondii infection in the studied
population groups.

Study Population. We studied 641 people living in rural
Durango State including 282 subjects of the general
population, 214 subjects of Huichol ethnicity, and 145
subjects of Mennonite ethnicity. Inclusion criteria for
enrollment were as follows: (1) living in rural Durango State,
(2) aged 14 years and older, and (3) who accepted to
participate in the survey. The socioeconomic status, gender,
and educational level of the subjects were not restrictive
criteria for enrollment. Concerning the 282 subjects of the
general population, they were sampled in three communities:
San Dimas, Villa Montemorelos, and Santa Clara, whereas
Huicholes were sampled in the community of Huazamota. For
its part, Mennonites were sampled in the community of
Nuevo Ideal. In total, the tested subjects included 408 females
and 233 males, aged 14–91 years (mean 40.30 ± 16.69 years).

Socio-Demographic, Clinical, and Behavioral
Characteristics of the Subjects. We obtained the sociodemo-
graphic, clinical, and behavioral characteristics of the study
population from archival Microsoft Excel files recorded in the
original studies [19–21]. Sociodemographic data included age,
gender, birthplace, occupation, socioeconomic status,
educational level, and type of flooring at home. Clinical data
included history of blood transfusion or solid organ
transplantation. Behavioral data included animal contacts
(cats, dogs, farm animals, and others), traveling (national or
international trips), type of meat consumed (beef, pork,
chicken, turkey, and others), degree of meat cooking (raw,
undercooked, or well done), consumption of unpasteurized
European Journal of Microbiology and Immunology 9(2019)3, pp. 91–93

First published online: 22 August 2019

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Toxocara and Rural Mexico
milk, untreated water, unwashed raw fruits or vegetables,
eating in restaurants or fast food outlets, and soil contact.

Detection of Anti-Toxocara IgG Antibodies. Anti-
Toxocara immunoglobulin G (IgG) antibodies were detected
in the sera of subjects using a commercially available enzyme
immunoassay “Toxocara” kit (Diagnostic Automation, Inc.
Calabasas, CA, USA). All assays were performed following
the manufacturer's instructions. We included in each assay the
negative and positive controls provided in the kit.
Seropositivity was considered when an absorbance reading
≥0.3 optical density units was obtained.

Statistical Analysis. We performed the statistical analysis
using the software Microsoft Excel, Epi Info version 7, and
SPSS version 20. We calculated the sample size using the
following parameters: a population size of 500,000, a
reference seroprevalence of 26.2% [18] as the expected
frequency of exposure, 4% of confidence limits, and a 95%
confidence level. The result of the sample size calculation was
464 subjects. We used the two-tailed Fisher's exact test to
assess the association of Toxocara seropositivity and the
sociodemographic, clinical, and behavioral characteristics of
the subjects studied. A P value <0.05 was considered
statistically significant.

Ethical Aspects. In the present study, we analyzed only
archival serum samples and data obtained in the previous
studies. The original surveys were approved by Institutional
Ethics Committees [19–21].

Results

Three (0.5%) of the 641 subjects tested were positive for
anti-Toxocara IgG antibodies. Of the 3 Toxocara seropositive
subjects, 2 were females, aged 19 and 39 years, and one was
male, aged 59 years. The occupations of these 3 seropositive
subjects were as follows: a student, a housewife, and an agri-
culturist. They had contacted with dogs, cleaned cat excre-
ment, consumed unwashed raw fruits, contacted soil, or lived
in a house with soil floors. Seroprevalence of Toxocara infec-
tion was similar among the 3 groups of population studied:
0.4% for the general population, 0.9% for Huicholes, and
0.0% for Mennonites (P = 0.41). The Toxocara seropositivity
rate did not vary (P > 0.05) with respect to sociodemographic
characteristics of the study population including age, gender,
birthplace, occupation, socioeconomic status, educational
level, and type of flooring at home. Concerning clinical char-
acteristics, none of the Toxocara seropositive individuals had
a history of blood transfusion or solid organ transplantation.
None of the behavioral characteristics analyzed including ani-
mal contacts, traveling, type of meat consumed, degree of
meat cooking, consumption of unpasteurized milk, untreated
water, unwashed raw fruits or vegetables, eating in restaurants
or fast food outlets, and soil contact was associated with Toxo-
cara seropositivity rate (P > 0.05).

Discussion

The seroepidemiology of Toxocara infection in rural Mex-
ico has been sparsely studied so far. Therefore, in the current
study, we sought to determine the seroprevalence of Toxocara
infection in several communities in rural Durango State, Mex-
ico. We found a low (0.5%) seroprevalence of Toxocara infec-
tion in people living in rural areas of Durango State. This
finding was unexpected since living in rural areas is consid-
ered as a risk factor for Toxocara exposure in several coun-
tries in Asia [12, 14, 15, 17], Africa [13, 16], and Europe
[17]. The Toxocara seroprevalence found in our study is lower
than those reported in rural populations in Brazil (71.8%)
92
[22], Gabon (59.9%) [13], Argentina (23%–31.6%) [23, 24],
Poland (56.2%) [17], Korea (5%) [25], India (6.4%) [26], Bo-
livia (34%) [27], the Slovak Republic (17.09%) [28], and Ven-
ezuela (25.6%) [29]. In addition, the seroprevalence found in
our study is lower than the 26.2% Toxocara seroprevalence
reported in Tepehuanos in rural Durango, Mexico [18]. In fact,
the seroprevalence found in our study is the lowest ever
reported in rural communities. It is not clear why the seroprev-
alence in rural communities in Durango found in this study is
lower than those reported in similar populations elsewhere. It
is possible that the rate of Toxocara infection in dogs and cats
and soil contamination with Toxocara in the rural communi-
ties explored was low. We cannot rule out previous deworm-
ing in cats and dogs to reduce parasite transmission in the
communities studied. However, we did not obtain information
about deworming in animals in the communities studied. We
looked for socioeconomic, clinical, and behavioral factors as-
sociated with Toxocara infection in people in rural Durango;
however, statistical analysis showed that none of the character-
istics studied was associated with Toxocara infection. The
three Toxocara seropositive individuals found in the current
study had factors associated with Toxocara infection including
contact with dogs, cleaning cat excrement, consumption of un-
washed raw fruits, and soil contact. However, the lack of asso-
ciations between Toxocara seroreactivity and the
characteristics of the study population found in this study was
probably due to the very low number of Toxocara seropositive
individuals found. This low rate of Toxocara seropositivity
was certainly a limitation of the survey. Additional studies
with large sample sizes to determine risk factors associated
with Toxocara exposure of people in rural Durango are
needed.

In summary, we demonstrate a low rate of Toxocara expo-
sure among people living in rural Durango State. The sero-
prevalence found is lower than those reported in people living
in rural setting in other countries. Risk factors associated with
Toxocara exposure in rural Mexico remain to be determined.

Funding Sources

This study was financially supported by Juárez University
of Durango State.

Authors' Contributions

CAE designed the study protocol, performed the laboratory
tests and data analysis, and wrote the manuscript. AOAF and
GAAF performed the data analysis and reviewed the
manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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