259
Neotrop. Helminthol., 8(2), 2014
2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
FACTORS ASSOCIATED WITH CONTAMINATION OF PUBLIC PARKS (HUÁNUCO, PERÚ)
BY TOXOCARA CANIS EGGS AND OTHER ENDOPARASITES OF ZOONOTIC IMPORTANCE
FACTORES ASOCIADOS A LA CONTAMINACIÓN DE PARQUES PÚBLICOS (HUÁNUCO,
PERÚ) CON HUEVOS DE TOXOCARA CANIS Y OTROS ENDOPARASITOS DE IMPORTANCIA
ZOONOTICA
1 1 1 1
Eddyson Montalvo-Sabino , Fermin Cipriano-Fonseca , Edith Marcelo-Andrade , Doila Milagros Rosas-Jara , Wendy Mike
1 1 1 1
Mines-Huaman , Luz Nathaly Capcha-Tucto , Carla Chavez-Chavez , Branco Benites-Mendoza , Maribel Sandoval-
1 1 2 2,3 4,5
Tolentino , Carlos Alberto Pineda-Castillo , Jorge Cárdenas - Callirgos , Eric J. Wetzel & José Iannacone
Abstract
Key words: Ancylostoma - contamination by eggs - parasite - public parks - Toxocara.
Suggested citation: Montalvo-Sabino, E, Cipriano-Fonseca, F, Marcelo-Andrade, E, Rosas-Jara, DM, Mines-Huaman, WM,
Capcha-Tucto, LN, Chávez-Chávez, C, Benites-Mendoza, B, Sandoval-Tolentino, M, Pineda-Castillo, CA, Cárdenas -
Callirgos, J, Wetzel, EJ & Iannacone, J. 2014. Factors associated with contamination of public parks (Huanuco, Peru) by
Toxocara canis eggs and other endoparasites of zoonotic importance. Neotropical Helminthology, vol. 8, no. 2, July-Dec, pp.
259-268.
1Escuela Académico Profesional de Medicina Veterinaria, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Hermilio Valdizán,
2
Huanuco, Perú. Wabash Global Health Initiative, Wabash College, Crawfordsville, Indiana, US.
3Department of Biology, Wabash College, Crawfordsville, Indiana, US.
4 Laboratorio de Ecofisiología Animal (LEFA). Facultad de Ciencias Naturales y Matemática (FCNNM).
Universidad Nacional Federico Villarreal (UNFV). El Agustino, Lima, Perú.
5 Facultad de Ciencias Biológicas. Universidad Ricardo Palma (URP). Santiago de Surco, Lima, Perú.
E-mail: joseiannacone@gmail.com/jmcardenasc@gmail.com/eddysonmont@gmail.com
The objective of this work was to evaluate the contamination of public parks in the district of
Huánuco, Perú with eggs of Toxocara canis. 32 soil samples were taken in each of 11 parks for a
total of 352 samples in May and June of 2014. Parks were selected at random. In each park, 2-3 kg
soil was collected according to the double “W” method. Flotation with a saturated sugar solution
was used. Samples were considered positive when at least one egg of T. canis was found. Of the 11
parks sampled, T. canis eggs were found in 90.9%. Seven parasites were found along with T. canis
in the soil. The sequence of parasite prevalence was in the following descending order: T. canis >
Strongylus type eggs of Ancylostoma caninum > A. caninum larvae = Blastocystis hominis >
Trichuris vulpis = Entamoeba sp. > Capillaria sp. = Balantidium coli. Parasite richness was 2.45 ±
1.21 (1-4) parasites per public park. A significant positive correlation was observed between the
area of public parks and parasite richness per public park. No association was found between the
condition of the public park and it being positive for T. canis. A dendrogram of similarity of
association of parasites present in the 11 public parks showed a greater association between the
Strongylus egg type and larvae of A. caninum. Also, a greater similarity existed between T. vulpis,
B. coli, Entamoeba sp. and Capillaria sp. T. canis had the lowest similarity with the other parasitic
forms. An increase in the prevalence of T. canis was observed in comparison to the previous
decade as well as to the presence of other infective parasite stages of public health importance.
People and especially children could become contaminated while in public parks and sanitary
measures should be taken to control this zoonosis.
Montalvo-Sabino et al.
Factors associated with contamination of public parks by Toxocara canis eggs
260
Resumen
Palabras clave: Ancylostoma - contaminación por huevos - parásito - parques públicos – Toxocara.
El objetivo de este trabajo fue evaluar la contaminación de parques públicos del distrito de
Huánuco, Perú por huevos de Toxocara canis. En cada uno de los 11 parques fueron tomadas 32
muestras por lo que se evaluaron un total de 352 muestras de tierra en mayo y junio del 2014. La
selección de los parques fue al azar. De cada parque se recolectó 2 a 3 kg de tierra, según el método
de la doble “W”. Se usó el método de flotación con solución saturada de azúcar. Se consideró
positivo cuando se encontró al menos un huevo de T. canis por parque evaluado. De los 11 parques
muestreados se encontró huevos de T. canis en el 90,9%. Siete fueron las formas parasitarias
acompañantes a T. canis en el suelo. La secuencia de prevalencia parasitaria presentó el siguiente
orden descendente: T. canis > huevos tipo Strongylus de Ancylostoma caninum > larvas de A.
caninum = Blastocystis hominis > Trichuris vulpis = Entamoeba sp. > Capillaria sp. =
-1
Balantidium coli. La riqueza parasitaria fue de 2,45±1,21 (1 a 4) parásitos·parque público . Se
observó una correlación positiva significativa entre el área del parque público y la riqueza de
-1
parásitos·parque público . No se encontró asociación entre el estado de conservación del parque
público y la positividad con T. canis. Un dendrograma de similitud de asociación de los parásitos
presentes en los 11 parques públicos mostró una mayor asociación entre huevos tipo Strongylus y
larvas de A. caninum. También una mayor similitud entre T. vulpis, B. coli, Entamoeba sp. y
Capillaria sp. T. canis presentó la menor similitud con el resto de formas parasitarias. Se observó
un aumento en la prevalencia de T. canis en comparación a la década anterior, así como la
presencia de otros estadios infectivos de parásitos de importancia en salud pública. Las personas y
especialmente los niños pudieran contaminarse durante su estadía en los parques públicos y deben
tomarse medidas sanitarias para el control de esta zoonosis.
INTRODUCTION Barbadosa et al., 2008; Maragui et al., 2014).
These eggs remain in the soil until larval
development in 6 weeks, increasing the
possibility of infection to humans and causing a
risk to public health (Huapaya et al., 2009;
Armstrong et al., 2011; Trejo et al., 2012).
Toxocara larvae can migrate to the liver, lungs,
muscles and brain (Marques et al., 2012) and can
cause the syndromes of visceral larval migrans
(VLM) and ocular larval migrans (OLM)
(Martínez-Barbadosa et al., 2008; Bartosik &
Rzymowska, 2010; Marques et al., 2012;
Maragui et al., 2014).
Transmission of toxocariasis is mainly through
fecal matter disseminated in the environment
(Armstrong et al., 2011; Marques et al., 2012;
Maragui et al., 2014), to which humans have free
access through contact with the soils of parks
and gardens frequented by canids (Santarém et
al., 2012). The presence of environmental
contamination with Toxocara eggs is considered
Soils contaminated by eggs of helminth
parasites of animals may constitute a zoonotic
risk for humans and affect millions of people
(Romero-Núñez et al., 2011; Iannacone et al.,
2012; Marques et al., 2012; Traversa et al.,
2014). There have been many different parasitic
helminths with dogs (Canis lupus familiaris
Linnaeus, 1758) as definitive hosts which can be
transmitted to humans causing parasitic disease
(Rojas 2003).
Toxocariasis is a geohelminthic, mainly
asyptomatic, zoonotic disease caused by
Toxocara canis (Werner, 1782) and Toxocara
cati (Schrank, 1788) (Romero-Núñez et al.,
2011; Khazan et al., 2012; Trejo et al., 2012;
Maragui et al., 2014). Puppies with intestinal
infections with Toxocara can excrete eggs of this
helminth into the environment (Martínez-
Neotrop. Helminthol., 8(2), 2014
MATERIALS AND METHODS
to be the best indicator of infection risk to
humans (Marques et al., 2012; Santarém et al.,
2012; Saraei et al., 2012; Maragui et al., 2014).
The hookworms (Ancylostoma spp.) and
Trichuris vulpis (Froelich, 1789) are among the
most important helminth parasites in dogs in
environmental and clinical terms. Several
studies have demonstrated the relevance of these
two helminths in parks, green areas and beaches
(Bartosik & Rzymowska, 2010; Iannacone et
al., 2012; Traversa et al., 2014.).
High numbers of irresponsible dog owners, such
as owners who do not pick up the feces of their
pets, can lead to contamination by a large
quantity of fecal material disseminated in
recreation and leisure areas (Trejo et al., 2012).
Therefore, the aim of this study was to address
the following research question: What is the
state of soil contamination by eggs of T. canis in
public parks in the district of Huánuco, Perú?
Area and type of study
The study was descriptive, transversal and
comparative. Eleven parks in the district of
Huánuco, Huánuco, Perú (09°55'58?S;
76°14'30?W) were sampled (Table 1). Parks
were selected randomly. The average size of the
2
parks was 985.09 ± 240.69 m . 352 soil samples
were evaluated between May (n = 192) and June
(n = 160) of 2015, with 32 samples taken from
each of the 11 parks.
Soil samples
From each park was collected 2-3 kg of soil,
according to the double “W” method, which
consists of drawing in the sample area two “W”,
superimposed and inverted, with the length of
each “W” determined in steps and the earth
collected on each side of the “W”. Each sample
was taken at a depth of approximately 2.5 cm
and a diameter of 5 cm (Guerrero, 1975). The
samples were labeled with the name of the park
and placed in polyethylene bags, stored at room
temperature and taken to the laboratory for
parasitological analysis corresponding to the
environment (Zibaei et al., 2010; Armstrong et
al., 2011; Matesco et al., 2011; Khazan et al.,
2012). The method of Parodi Alcaraz was used
(concentration method by flotation without
centrifugation, using a supersaturated Benbrook
sugar solution) (Daprato et al., 2011; Maragui et
al., 2014). Soil samples were placed in a mortar
and the supersaturated sugar solution added and
mixed well, using the pestle to crush coarse
pieces. The obtained mixture was filtered
through a funnel with a metal filter into 15 ml
test tubes; the tubes were filled to form a
meniscus and then covered with a glass
coverslip. After 20 min the coverslip was
removed and the slide examined under a
microscope. Identification of Toxocara was
made according to their morphology and typical
size (Saraei et al., 2012). Samples were
considered positive when at least one egg of
Toxocara per sample was found (Harbinder et
al., 1997). Classification of eggs according to
their state of development, e.g., single cell, pre-
embryonated, and embryonated was not made.
Viability of eggs was also not evaluated
(Daprato et al., 2011; Romero-Núñez et al.,
2011). Similar parasitic forms present in each
sample (helminth eggs and larvae, protozoan
cysts) were analyzed according to specific
identification guides.
Condition of public parks
Public parks were classified in the following
manner: (1) Well preserved: parks entirely
covered (100%) by grass; (2) Moderately
preserved: parks approximately 50% covered by
grass; and (3) Poorly preserved: neglected parks
entirely without grass and with earth and sand
only (Huaraca, 2001).
Data analysis
Spearman's correlation (r ) between the area and
s
the condition of each public park was performed
and the parasite richness for each park
examined. The Chi-square statistic also was
used to associate park condition and prevalence
of T. canis. A dendrogram of similarity of
association (cluster analysis) of parasites found
in the public parks of Huánuco, Peru was
performed based on the algorithm of group pairs,
261
Montalvo-Sabino et al.
Factors associated with contamination of public parks by Toxocara canis eggs
using Ward's method with the respective
correlation coefficients.
Table 1 shows the presence of T. canis and other
forms of parasitic helminths and protozoans in
11 public parks in Huánuco. The sequence of
parasite prevalence presented the following
descending order: T. canis > Strongylus type
eggs of A. caninum > hookworm larvae (A.
caninum) = Blastocystis hominis (Swayne &
Britton, 1849) Brumpt, 1912 > T. vulpis =
Entamoeba sp. > Capillaria sp. = Balantidium
coli Malmsten, 1857 (Table 1). The parasite
richness was 2.45 ± 1.21 (1-4) parasites per
public park. The sequence of the parasite
richness of public parks provided the following
descending order: 23 de febrero = Plaza mayor =
Amarilis > San Pedro (Ramón Castilla) =
Puelles > San Cristobal = San Sebastian = San
Francisco > Santo Domingo = Heroes
Huanuqueños = San Pedro (Infantil de tránsito)
(Table 1). A significant positive correlation
between the area of the public park and the
parasite richness per public park (r = 0.74; p =
s
0.009) was observed.
Of the 11 parks, 3 were well preserved, 7 were
moderately preserved and 1 was in poor
condition (Table 2). The well preserved and
poorly preserved public parks showed 100%
positivity and the moderately preserved showed
only 85.71% (Table 2). No association was
found between the condition of the park and the
2
positivity with T. canis (X = 2.29; p = 0.32).
Likewise, no correlation between park condition
and parasite richness was seen (r = 0.43; p =
s
0.19).
Figure 1 shows a dendrogram of similarity of
association among the parasites co-occurring
with T. canis in the 11 public parks of Huánuco
(correlation coefficient of cluster analysis =
0.87). A greater association between Strongylus
type eggs of A. caninum and larvae of A.
caninum was seen. Also, there was a greater
similarity between T. vulpis and B. coli, and
between Entamoeba sp. and Capillaria sp. T.
canis had the lowest similarity with the rest of
the parasitic forms present in the public parks
based on the method of Ward.
RESULTS
4.8
4.4
4.0
3.6
3.2
2.8
2.4
2.0
1.6
1.2
0.8
0.4
0.0
Similarity
Tox
Stro
Unc
Blas
Tri
Bal
Cap
Ent
Figure 1. Dendrogram of cluster analysis similarity of parasites found in public parks in Huanuco, Peru based on the algorithm of
group pairs according to Ward's method (r = 0.87). Tox = Toxocara canis. Stro = Strongylus egg type of Ancylostoma caninum. Tri
= Trichuris vulpis. Cap = Capillaria sp. Unc = larva of A. caninum. Blas = Blastocystis hominis. Ent = Entamoeba sp. Bal =
Balantidium coli.
262
Neotrop. Helminthol., 8(2), 2014
Public Park área
m2
EC Tox
Stro
Tri
Cap
Unc
Blas
Ent
Bal
Richness
% MP
Plaza mayor 1100
1 +
+
+
+
4
37.5
Santo Domingo 970 2 +
1
50
San Cristóbal 650 1 +
+
2
34.7
San Sebastián 580 2 +
+
2
78.13
San Francisco (Cartagena) 980 2 +
+
2
53.13
Amarilis 1020
2 +
+
+
+
4
31.25
San Pedro (Ramón Castilla) 1000
2 +
+
+
3
62.50
San Pedro (Infantil de transito) 980 3 +
1
53.13
23 de febrero (tramo puente San Sebastián -
Cementerio) 1450
2 +
+
+
+
4
0
Héroes Huanuqueños (Tabaco)
876
2
+
1
56.25
Puelles (Los periodistas) 1230 1 + + + 3 12 50
Prevalence (%)
90.90
45.45
18.18
9.09
27.27
27.27
18.18
9.09
Table 1. Surface area, condition and presence of parasites in 11 public parks of the district of Huánuco, Huánuco, Perú. Tox = Toxocara canis. Stro = Strongylus egg
type of Ancylostoma caninum. Tri = Trichuris vulpis. Cap = Capillaria sp. Unc = larva of A. caninum. Blas = Blastocystis hominis. Ent = Entamoeba sp. Bal =
Balantidium coli. EC = Condition. 1 = Well preserved. 2 = Moderately preserved. 3 = Poorly preserved. % MP = percentage of samples positive for T. canis. + =
Presence of the parasite.
263
Table 2. Number and frequency of positive parks – contaminated with Toxocara canis according to their condition in
the district of Huánuco, Huánuco, Perú.
Montalvo-Sabino et al.
Factors associated with contamination of public parks by Toxocara canis eggs
Condition
# of parks (%) Positive (%)
Well preserved 3 27.27 3 100
Moderately preserved 7 63.63 6 85.71
Poorly preserved 1 9.09 1 100
Total
11 100 10 90.90
2
X = 2.29, P =0.32.
DISCUSSION
Several investigations have determined the soil
contamination of public parks in different
socioeconomic levels worldwide (Khazan et al.,
2012; Iannacone et al., 2012; Saraei et al., 2012;
Sudhakar et al., 2013). The contamination by
eggs of T. canis (90.9%) is very high in the
district of Huánuco, Huánuco, Peru and could
cause infection in people who use public parks
and recreational áreas (Khazan et al., 2012;
Sudhakar et al., 2013).
The identification of T. canis eggs in the soil of
public parks of Huánuco, Perú is a bioindicator
of the presence of infected dogs that defecate in
these areas of rest and relaxation, and a high
source of contamination to people (Saraei et al.,
2012; Trejo et al., 2012; Sudhakar et al., 2013).
Children engaged in recreational activities in
these parks are at a higher vulnerability and
epidemiological risk caused by this helminth
(Khazan et al., 2012; Sudhakar et al., 2013).
A positive correlation was observed between the
area of the public park and the parasite richness
per public park. Zibaei et al. (2010) found that
2
parks more than 10000 m were contaminated
more than those of smaller size. Conversely,
Trejo et al. (2012) in México City found that the
size of green area had no influence on the
presence and viability of eggs of Toxocara sp.
A high association between Strongylus type of
eggs of A. caninum and larvae of A. caninum was
seen. Traversa et al. (2014) indicated that
Ancylostoma spp. is, after Toxocara, the species
most prevalent in parks and gardens with an
average prevalence in 7 investigations in
America of 39.02%. The high association found
between the eggs and larvae of A. caninum in the
parks of Huánuco is evidence of continuous
contamination with this geohelminth.
With respect to the condition of the public parks,
6 parks were moderately preserved, 3 parks were
well preserved and one park poorly preserved;
these were contaminated with T. canis eggs,
accounting for 85.71% (6/7), 100% (3/3) and
100% (1/1), respectively. This means that there
was no relation between the presence of T. canis
eggs and the condition of the parks. Our results
are in contrast to the information found by
Huaraca (2001), who noted that the moderately
preserved, well preserved, and poorly preserved
parks were contaminated at 100% (2/2); 77.7%
(7/9) and 0% (0/1), respectively, possibly due to
the preference of canids to defecate in areas
more carefully constructed. Soils that retain
moisture are better for the developmental cycle
of the eggs of T. canis in contrast with the parks
that had only soil and cement (Marques et al.,
2012). In addition, Pomé et al. (2013) noted that
the risk factors for contamination by Toxocara
are: public lighting, no use of trash containers,
presence of green areas, dog-walking without a
leash and outside sale of prepared foods.
Several environmental and sociocultural factors
may influence the presence of Toxocara in soils
of public parks such as: weather, soil texture,
season, latitude, altitude, sunshine, geographic
location, procedure of soil collection, sampling
depth, number and volume of samples, and size
of the park, among others (Zibaei et al., 2010;
264
Neotrop. Helminthol., 8(2), 2014
Daprato et al., 2011; Matesco et al., 2011;
Santarém et al., 2012; Sudhakar et al., 2013).
Inadequate official sanitary measures in relation
to responsible pet ownership that avoids or
reduces the presence of dog feces in public parks
could explain the high levels of contamination
with Toxocara (Khazan et al., 2012; Santarém et
al., 2012). In the territory of Peru, there is the
Supreme Decree No. 006-2002-SA with its Rule
of Law No. 27596 that regulates responsible
ownership of dogs, and the municipal ordinance
No. O4:2014-MPH-LL that standardizes the
ownership, protection and control of dogs in the
district of Huánuco, Huánuco, Perú. In
particular, in this last regulation the owners are
obliged not to permit their dogs to roam or leave
their homes and should properly remove their
feces or droppings. Our results show that the
regulations regarding responsable dog
ownership are not being fulfilled efficiently in
the district of Huánuco, Huánuco, Perú.
The percentage contamination with T. canis eggs
(90.9%) in this study showed an increase in the
last decade in relation to that previously
recorded in the same locality (Rafael, 2000 cited
by Iannacone et al., 2012; Pujay, 2000 cited by
Iannacone et al., 2012; Huaraca, 2001). This
could be due to the different times of year in
which samples were collected, apparently being
favorable in the present case in which the rainy
season was extended until May, while previous
surveys were conducted mainly during the dry
season (Daprato et al., 2011; Santarém et al.,
2012). Iannacone et al. (2012), in an analysis of
the prevalence of eggs of Toxocara sp. in parks
and recreational areas in several Latin
Americans countries, found a lower prevalence
in Peruvian Andean localities of high altitude
(Cusco, 32.6% at 3399 masl and Puno, 25% at
3827 masl) in comparison with Huánuco (90.9%
at 1894 masl).
Among the helminths reported in this study, A.
caninum has been reported in Peru in dogs and
domestic cats, as well as in the fox Lycalopex
culpaeus (Molina, 1782) in several locations
such as Cajamarca; Cusco; Huancavelica;
Chincha (Ica), Huancayo (Junin); Huarochiri,
Lima, Tayacaja, Yauyos (Lima); Iquitos,
Maynas (Loreto); Tahuamanu (Madre de Dios);
and Puno (Puno) (Sarmiento et al. (1999).
Prevalences have been seen up to 12% in Lima
and 52% in the Mantaro Valley (Leguia, 2002),
and its importance in public health has been
recognized with the clinical symptoms known as
cutaneous larval migrans (Leguía, 2002).
Trichuris vulpis has been reported in the
departments of Cusco and Lima (Sarmiento et
al., 1999), with a 10% prevalence found in Lima
(Leguía, 2002). Their eggs are very resistant to
adverse environmental conditions and remain
viable for years (Leguía, 2002) while their
zoonotic potential is still under discussion
(Traversa, 2011). Capillaria sp. has been
reported in several species of birds and domestic
and wild mammals in several provinces of Peru
(Sarmiento et al., 1999); in the case of Calodium
hepaticum (Bancroft, 1893) Moravec, 1982
(syn. Capillaria hepatica), various mammals,
including mice and rats as well as some
carnivores such as dogs and cats, are involved in
their life cycle (Taylor et al., 2007), with their
zoonotic potential recognized in our area
(Tantalean, 1994).
Among the protozoa B. coli has been reported in
pigs in Lima and Callao (Zaldivar, 1991) and in
other countries in various domestic and wild
mammals, including dogs and cats (Taylor et al.,
2007), besides being reported in several clinical
cases in the Peruvian population (Pamo et al.,
1999). Blastocystis hominis has been reported in
a wide variety of animals (Taylor et al., 2007)
including domestic dogs (Wang et al., 2013),
proving its zoonotic potential and having
reported human cases in our country (Salinas
&Vildazola Gonzales, 2007). Finally,
Entamoeba sp. also has been reported from a
wide variety of animals; the species most
important in public health, E. histolytica
Schaudinn, 1903, has been reported sporadically
in domestic animals like dogs (Taylor et al.,
2007) and is present in the human popuation of
Perú (Cornejo et al., 1999).
Several of these parasites have not been reported
previously contaminating parks of Peru and their
265
ACKNOWLEDGMENTS
BIBLIOGRAPHIC REFERENCES
Montalvo-Sabino et al.
Factors associated with contamination of public parks by Toxocara canis eggs
presence could be a bioindicator that dogs and
cats, other domestic animals (such as rodents
and pigs), wild animals (e.g., wild pigeons,
possibly indicated by the presence of Capillaria
sp.) and even the likely presence of human feces
could explain our findings in the public parks of
the city of Huánuco.
Thanks to members of CEMEVET (Center for
the study of Veterinary Medicine) and
UNHEVAL-Universidad Hermilio Valdizán,
Huánuco- Peru for the collection of samples.
Also, thanks to Carlos Alberto Del Águila Pérez
and the entire team of the Wabash College
Global Health Initiative for their cooperation in
the planning and initiation of this project.
Armstrong, WA, Oberg, C & Orellana, JJ. 2011.
Bartosik, M & Rzymowska, J. 2010.
Cornejo, W, Espinoza, Y, Huiza, A, Alva, P,
Suárez, R, Sevilla C & Náquira, C. 1999.
Presencia de huevos de parásitos con
potencial zoonótico en parques y plazas
públicas de la ciudad de Temuco, Región
de La Araucanía, Chile. [Presence of
parasite eggs with zoonotic potential in
parks and public plazas in the city of
Temuco, La Araucania Region, Chile.]
Archivos de Medicina Veterinaria, vol.
43, pp.127-134.
Geohelminth eggs' contamination of the
parks and sandpits in Lublin area.
Annales Universitatis Mariae Curie-
Sklodowska Lublin- Polonia, vol. 23, pp.
61-66.
Prevalencia de E. histolytica y E. dispar
por microscopía y ELISA en muestras
fecales de una población urbano marginal
de Lima. [Prevalence of E. histolytica and
E. dispar by microscopy and ELISA in
fecal samples of a marginal urban
population of Lima.] Anales de la
Facultad de Medicina, vol. 60, pp. 124-28.
Persistencia de la
contaminación ambiental por huevos de
Toxocara cati en un espacio público.
Argentina. [Persistence of environmental
contamination by eggs of Toxocara cati in
a public space. Argentina.] Revista
Sapuvet de Salud Pública, vol. 2, pp. 23-
35. Estudio de la contaminación
de parques públicos de Lima
Metropolitana con huevos de Toxocara sp.
[Study of the contamination of public
parks of Metropolitan Lima with eggs of
Toxocara sp.] Tesis para optar el grado de
Bachiller en Medicina Veterinaria,
Universidad Nacional Mayor de San
Marcos (UNMSM). Lima, Perú.
Prevalence of Toxocara spp. eggs in the
soil of public and private places in
Ludhiana and Kellon area of Punjab,
India. International Symposia on
Veterinary Epidemiology and Economics
proceedings - ISVEE 8: Proceedings of
th
the 8 Symposium of the International
Society for Veterinary Epidemiology and
Economics, Paris, France. Epidémiologie
et Santé Animale, vol. 31-32, pp. 4-5.
Toxocariosis humana:
¿problema de Salud Pública? [Human
Toxocariasis: Problem of Public Health?]
Anales de la Facultad de Medicina, vol.
70, pp. 283-290.
Contaminación de parques
públicos con huevos de Toxocara sp.
[Contamination of public parks with eggs
of Toxocara sp.] Tesis Universidad
Hermilio Valdizán, Huánuco, Perú.
Contaminación de los suelos con
huevos de Toxocara canis en parques
públicos de Santiago de Surco, Lima,
Perú, 2007-2008. [Soil contamination
with eggs of Toxocara canis in public
parks of Santiago de Surco, Lima, Peru,
2007-2008.] Neotropical Helminthology,
vol. 6, pp. 97- 108.
Daprato, B, Cardillo, N, Kunic, M, Berra, Y &
Sommerfelt, I. 2011.
Guerrero, M. 1975.
Harbinder, S, Bali, HS & Arvinder, K. 1997.
Huapaya, HP, Espinoza, Y, Roldán, W &
Jiménez, S. 2009.
Huaraca, P. 2001.
Iannacone, J, Alvariño, L & Cárdenas-Callirgos,
J. 2012.
266
Neotrop. Helminthol., 8(2), 2014
Relación entre la presencia de Toxocara
sp. y la clasificación de parques
amigables en la ciudad de Abancay.
[Relation between the presence of
Toxocara sp. and the classification of
friendly parks in the city of Abancay].
Libro de Resúmenes del VII Congreso
Científico Internacional del Instituto
Nacional de Salud “Investigar para
construir Políticas Públicas en Salud” del
07 al 09 de noviembre del 2013. Instituto
Nacional de Salud, Lima, Perú. p. 17.
Nosoparasitosis de perros y
gatos peruanos. [Nosoparasitosis of
Peruvian dogs and cats.] Ed Martegraf.
Perú. 83 p.
Presencia y
viabilidad de Toxocara spp. en suelos de
parques públicos, jardines de casas y
heces de perros en Nezahualcóyolt,
México. [Presence and viability of
Toxocara spp. in soils of public parks,
gardens and feces of dogs in
Nezahualcóyolt, México.] Revista
Científica, FCV-Luz, vol. 21, pp. 195-
201.
Infección por Blastocystis. [Infection by
B l a s t o c y s t i s . ] R e v i s t a d e
Gastroenterología del Perú, vol. 27, pp.
264-74.
Contamination of public parks in
Presidente (Sao Paulo, Brasil) by
Toxocara spp. eggs. Revista Brasileira de
Parasitologia, Jaboticabal, vol. 21, pp.
323-325.
Contamination of soil and grass to
Toxocara spp. eggs in public parks of
Qazvin, Iran. Asian Pacific Journal of
Tropical Biomedicine, vol. S2, S1156-
S1158.
Nemátodos parásitos del hombre y de los
animales en el Perú. [Nematode parasites
of humans and animals in Peru.] Revista
Rojas, M. 2003.
Romero-Nuñez, C, Mendoza-Martínez, D,
Bustamante, LP, Crosby-Galván, MM &
Ramírez-Durán, N. 2011.
Salinas, JL & Vildozola González, H. 2007.
Santarém, VA, Pereira, VC & Alegre, BCP.
2012.
Saraei, M, Zakilo, M, Tavazoei, Y,
Jahanihashemi, H & Shahnazi, M. 2012.
Sarmiento, L, Tantaleán, M & Huiza, A. 1999.
Khazan, H, Khazaei, M, Tabaee, SJS & Mehrabi,
A. 2012.
Leguía, G. 2002.
Maraghi, S, Jafari, KM, Sadjadi, SM, Latifi, SM
& Zibaei, M. 2014.
Marques, JP, Guimarães, CR, Vilas Boas, A,
Carnaúba, PU & Moraes. 2012.
Martínez-Barbabosa, I, Gutiérrez-Cárdenas,
EM, Alpízar-Sosa, EA, Pimienta-Lastra,
RJ. 2008.
Matesco, VC, Rott, MB & Bohrer, MM. 2011.
Pamo O, Figueroa, M & Ruíz, J. 1991.
Pomé, AAV, Pinto, CC & Cárdenas, RB. 2013.
Prevalence of Toxocara spp.
eggs in public parks in Tehran city, Iran.
Iranian Journal of Parasitology, vol. 7, pp.
38-42. Enfermedades parasitarias de
perros y gatos. [Parasitic diseases in dogs
and cats.] Epidemiología y control. Ed de
Mar. Perú. 155p.
Study on the
contamination of Abdan public parks soil
with Toxocara spp. eggs. Journal of
Environmental Health Science &
Engineering, vol. 12, pp. 86.
Contamination of public parks and
squares from Guarulhos (Sao Paulo State,
Brazil) by Toxocara spp. and
Ancylostoma spp. Revista do Instituto de
Medicina Tropical de São Paulo, vol. 54,
pp. 267-271.
Contaminación parasitaria en
heces de perros, recolectadas en calles de
la ciudad de San Cristóbal de Las Casas,
C h i a p a s , M é x i c o . [ P a r a s i t i c
contamination in feces of dogs, collected
in streets of the city of San Cristóbal de
Las Casas, Chiapas, México.] Veterinaria
México, vol. 39, pp. 173-180.
Comparação entre métodos de centrífugo
flutuação utilizados para a recuperação
de ovos de helmintos em amostras de
areia. [Comparison of centrifugal
flotation methods used for the recovery of
helminth eggs in sand samples.] Revista
de Patologia Tropical, vol. 40, pp. 323-
330.
Balantidiasis: Reporte de cuatro casos y
revisión de la casuística de los hospitales
de Lima. [Balantidiasis: Report of four
cases and review of the cases of the
hospitals of Lima.] Revista Médica
Herediana, vol. 2, pp. 195-7.
267
Montalvo-Sabino et al.
Factors associated with contamination of public parks by Toxocara canis eggs
Trejo, CAC, Romero-Nuñez, C, García-
Contreras, AC & Mendoza-Barrera, GE.
2012.
Wang, W, Cuttell, L, Bielefeldt-Ohmann, H,
Inpankaew, T, Owen, H & Traub, RJ.
2013.
Zaldivar, R. 1991.
Zibaei, M, Abdollahpour, F, Birjandi, M &
Firoozeh, F. 2010.
Soil contamination by Toxocara
spp. eggs in a University in Mexico city.
Revista Brasileira de Parasitologia
Veterinaria, vol. 21, pp. 298-300.
Diversity of Blastocystis subtypes in
dogs in different geographical settings.
Parasites & Vectors, vol 6, pp.215.
Zooparasitos de interés
veterinario en el Perú. [Zooparasites of
veterinary interest in Peru.] Ed Maijosa.
Peru. 252p.
Soil contamination
with Toxocara spp. eggs in the public
parks from three areas of Khorram Abab,
Iran. Nepal Medical College Journal, vol.
12, pp. 63-65.
Peruana de Parasitología, vol. 14, pp. 9-
65.
Prevalence of Toxocara species
eggs in soil samples of public health
importance in and around Bareilly, Uttar
Pradesh, India. Vet World, vol. 6, pp. 87-
90. Nuevos helmintos de
importancia medica en el Perú. [New
helminths of medical importance in Peru.]
Revista Peruana de Medicina Tropical
UNMSM, vol. 8, pp. 87-91.
Veterinary Parasitology. Ed Blackwell
Publishing Ltd. UK. 874p.
Are we paying too much
attention to cardio-pulmonary nematodes
and neglecting old-fashioned worms like
Trichuris vulpis?. Parasites & Vectors,
vol 4, pp.32.
Environmental contamination by canine
geohelminths. Parasites & Vectors, vol. 7,
pp.67.
Sudhakar, NR, Samanta, S, Sahu, S, Raina, OK,
Gupta, SC, Madhu, DN & Kumar, A.
2013.
Tantaleán, M. 1994.
Taylor, MA, Coop, RL & Wall, RL. 2007.
Traversa, D. 2011.
Traversa, D, di Regalbono, AF, di Cesare, A, La
Torre, F, Drake, J & Pietrobelli, M. 2014. Received July 1, 2014.
Accepted August 7, 2014.
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