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ASSESSMENT OF THE PRESENCE OF Toxocara EGGS IN SOILS OF AN ARID AREA IN CENTRAL-WESTERN ARGENTINA

Evaluación de la presencia de huevos de Toxocara en suelos de una zona árida en la región centro-oeste Argentina

Abstracts

With the aim of studying the contamination of soils with eggs of Toxocara spp. in an arid area in the central-western region of Argentina, 76 soil samples were collected from 18 towns belonging to six provinces of central-western Argentina. They were processed by the centrifugal flotation method. No eggs of Toxocara spp. were found. It can be concluded that the negative results are directly related to the characteristics of the environment and climate present in the studied area. The finding of eggs in soils depends on several factors: the presence of canine or feline feces, the hygienic behavior of pet owners, the presence of stray animals without veterinary supervision, the weather and environmental conditions, and laboratory techniques used; and all these circumstances must be considered when comparing the results found in different geographical regions. In order to accurately define the importance of public spaces in the transmission of infection to humans, it is important to consider the role of backyards or green spaces around housing in small towns, where the population is not used to walking pets in public spaces, and in such cases a significant fraction of the population may acquire the infection within households.

Toxocariosis; Soil contamination; Zoonotic; Environment; Laboratory method


Con el objetivo de estudiar la contaminación de los suelos con huevos de Toxocara spp, se obtuvieron 76 muestras de suelo de 18 pueblos pertenecientes a 6 provincias del centro-oeste de Argentina. Las muestras fueron procesadas por el método de centrifugación-flotación. No se encontraron huevos de Toxocara spp. en ninguna de las muestras de suelo. Llegamos a la conclusión de que los resultados negativos podrían estar en relación directa con las características ambientales y climáticas presentes en el área estudiada. El hallazgo o no de huevos en el suelo depende de varios factores: la presencia de heces de caninos o felinos, el comportamiento de los dueños de mascotas, la presencia de animales abandonados y sin control veterinario, las condiciones climáticas y ambientales y las técnicas de laboratorio utilizadas. Todas estas circunstancias deben ser consideradas cuando se comparan los resultados encontrados en diferentes regiones geográficas. Con el fin de definir la importancia que tienen los espacios públicos en la transmisión de la infección a los humanos, se debería considerar el papel que tienen los patios y veredas de las viviendas en las ciudades pequeñas, donde la población no acostumbra a pasear mascotas en parques y plazas, y en esos casos, la población puede adquirir la infección dentro de los hogares.


INTRODUCTION

Toxocariosis is the most frequently reported zoonotic geohelminthic infection worldwide and is caused by Toxocara canis or Toxocara cati. Although it has not yet been clearly demonstrated which one of these species is the most relevant in the epidemiology of the infection, due to the inability of routine procedures to distinguish one species from the other33. Borecka A. Differentiation of Toxocara spp. eggs isolated from the soil by PCR-linked RFLP. Helminthologia. 2004;41:185-7.,99. Jacobs DE, Zhu X, Gasser RB, Chilton NB. PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Trop. 1997;68:191-200..

The life cycle of Toxocara shows the importance of soil in the transmission of infection to humans. The eggs expelled in pets' feces complete their maturation in the soil, until full development of infective larvae, and thus, they contaminate the surface of the soil1818. Radman NE, Archelli SM, Fonrouge RD, del V Guardis M, Linzitto OR. Human toxocarosis. It's seroprevalence in the city of La Plata. Mem Inst Oswaldo Cruz. 2000;95:281-5.. Public places like parks, sidewalks, beaches etc are commonly shared by people and dogs as places for recreation and transit, and, therefore, in order to understand the epidemiological pathways of various zoonoses in relation with the environment, the rate of parasitic intestinal infestation of pets is usually studied and related to soil contamination1313. Milano AMF, Oscherov EB. Contaminación de aceras con enteroparásitos caninos en Corrientes, Argentina. Parasitol Latinoam. 2005;60:82-5..

Although Toxocara spp. is described as an agent present worldwide, no reports exist regarding the contamination of recreational public areas in the central-western region of Argentina; for this reason, the aim of this work is to assess the contamination of soils with eggs of Toxocara spp. in that area.

MATERIALS AND METHODS

Study Area: Soils from the central-western region of Argentina were studied. This is an extensive area located between the parallels 28 and 32 of SL and the meridians 64 and 68 of WL. The climate in this region is dry, arid, with cold winters (an average annual temperature of less than 12 °C) and warm summers, with an important daily temperature amplitude, with little snow and/or rainfall (< 200 mm per year), dry winds and scarce vegetation. Historical records of temperature and precipitation averages for the month of September in this region are: minimum temperature 7 °C, average temperature 15 °C, maximum temperature 23 °C and average rainfall 12 mm1616. National Weather Service. Available from: http://www.smn.gov.ar/
http://www.smn.gov.ar/...
.

Children's recreational sites were selected in the following locations: the city of Mendoza and the towns of La Paz and Uspallata in the province of Mendoza; the towns of Caucete and St. Lucia in the province of San Juan; the city of Merlo in the province of San Luis; the city of La Rioja and the towns of Patquía, Chepes and Anillaco in the province of La Rioja; the city of San Fernando and the town of Valle Viejo in the province of Catamarca; and the towns San Antonio de Arredondo, El Condor, Nono, Las Rabonas, San Javier and Luyaba in the western region of the province of Cordoba (Fig. 1).

Fig. 1
Map of Argentina showing the provinces composing the central-western region.

Sampling: In September 2012, 76 soil samples were collected from 35 different sites in 18 towns belonging to six provinces of the central-western region of Argentina.

Samples were taken from sandboxes and children's playgrounds in squares and parks, and from other sites where recreational use was evident. Samples consisted of 200-250g of dry soil collected from every square meter of the site. Bare ground with little drainage and no evidence of fouling by dogs or cats were selected. Samples were kept in the dark at room temperature until processing22. Alonso JM, Luna AC, Fernández GJ, Bojanich MV, Alonso ME. Huevos de Toxocara en suelos urbanos destinados a recreación en una ciudad Argentina. Acta Bioquím Clín Latinoam. 2006;40:219-22..

Methodology: Soil samples were carefully mixed and sieved through a 4 mm2 mesh to remove large stones and plant residues and were divided into four aliquots of 5 g each. The aliquots were washed with tap water twice, centrifuged and the supernatants were discarded. Pellets were suspended in two different flotation solutions: two in saturated ClNa solution (δ 1.205)1717. Quinn R, Smith HV, Bruce RG, Girwood RW. Studies on the incidence of Toxocara and Toxascaris spp. ova in the environment. 1. A comparison of flotation procedures for recovering Toxocara spp. ova from soil. J Hyg (Lond). 1980;84:83-9. and two in saturated sucrose solution (δ 1.27)2323. Ybáñez MR, Garijo M, Goyena M, Alonso FD. Improved methods for recovering eggs of Toxocara canis from soil. J Helminthol. 2000;74:349-53.. Each suspension was mixed and centrifuged at 2000 g for 10 min, and then completed with solution to the formation of meniscus and covered with a cover slip. After 20 min they were observed under light microscopy. No egg count was performed and the data were recorded as presence/absence of eggs11. Alonso JM, Stein M, Chamorro MC, Bojanich MV. Contamination of soils with eggs of Toxocara in a subtropical city in Argentina. J Helminthol. 2001;75:165-8..

RESULTS AND DISCUSSION

No eggs of Toxocara spp. were found in any of the 76 samples studied.

The recovery of T. canis eggs from soil samples depends on several factors, such as environmental conditions (including light, temperature, humidity and air quality)44. Celis Trejo CA, Romero Núñez C, García Contreras AC, Mendoza Barrera GE. Soil contamination by Toxocara spp. eggs in a University in Mexico City. Rev Bras Parasitol Vet. 2012;21:298-300., the sampling site, the laboratory method employed etc2121. Santarém VA, Magoti LP, Sichieri TD. Influence of variables on centrifuge-flotation technique for recovery of Toxocara canis eggs from soil. Rev Inst Med Trop Sao Paulo. 2009;51:163-7.. Toxocara spp. eggs require a period of time under appropriate environmental conditions to become infective to definitive and paratenic hosts. Temperature and humidity are important factors known to affect the levels of development in soil1010. Keegan JD, Holland CV. A comparison of Toxocara canis embryonation under controlled conditions in soil and hair. J Helminthol. 2013;87:78-84.. MIZGAJSKA stated that, in arid conditions, with exposure to sunlight and temperatures below 10 °C, Toxocara eggs die. It should be noted that sampling of this work was carried out in late winter1515. Mizgajska H. Eggs of Toxocara spp. in the environment and their public health implications. J Helminthol. 2001;75:147-51..

In the environment, feces carrying hundreds of thousands of eggs are dispersed by the physical action of: trampling, rain, wind, vectors etc., spreading the eggs' parasitic forms. The presence of Toxocara eggs is an indicator of canine fecal contamination above ground, resulting in the exposure of every human in the local population regardless of sex, age or socioeconomic status88. Fonrouge R, Guardis M, Radman NE, Archelli SM. Contaminación de suelos con huevos de Toxocara sp. en plazas y parques públicos de la ciudad de La Plata, Buenos Aires, Argentina. Bol Chil Parasitol. 2000;55:83-5..

In Argentina, urban contamination by Toxocara eggs has been extensively described in the central areas of large and medium-size cities due to the poor standards of care and irresponsible pet ownership (Table 1). The following surveys should also be mentioned: MINVIELLE et al. on public parks and sidewalks in the city of La Plata1414. Minvielle MC, Pezzani BC, Basualdo Farjat JA. Frecuencia de hallazgo de huevos de helmintos en materia fecal canina recolectada en lugares públicos de la ciudad de La Plata, Argentina. Bol Chil Parasitol. 1993;48:63-5.; FONROUGE et al.88. Fonrouge R, Guardis M, Radman NE, Archelli SM. Contaminación de suelos con huevos de Toxocara sp. en plazas y parques públicos de la ciudad de La Plata, Buenos Aires, Argentina. Bol Chil Parasitol. 2000;55:83-5. and CÓRDOBA et al.66. Córdoba A, Ciarmela ML, Pezzani BC, Gamboa MI, De Luca MM, Minvielle MC, et al. Presencia de parásitos intestinales en paseos públicos urbanos en La Plata Argentina. Parasitol Latinoam. 2002;57:25-9., who also studied public walks in La Plata, RUBEL & WISNIVESKY in Buenos Aires1919. Rubel D, Wisnivesky C. Magnitude and distribution of canine fecal contamination and helminth eggs in two areas of different urban structure, greater Buenos Aires, Argentina. Vet Parasitol. 2005;133:339-47.; MARTIN & DEMONTE in Santa Fe1111. Martin U, Demonte M. Urban contamination with zoonotic parasites in the central region of Argentina. Medicina (B Aires). 2008;68:363-6.; SORIANO et al. in the city of Neuquén2222. Soriano SV, Pierangeli NB, Roccia I, Bergagna HFJ, Lazzarini LE, Celescinco A, et al. A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquén, Patagonia, Argentina. Vet Parasitol. 2010;167:81-5.; and SÁNCHEZ THEVENET et al. on the contamination of canine feces found on sidewalks in the cities of Comodoro Rivadavia (Province of Chubut)2020. Sánchez Thevenet P, Jensen O, Mellado I, Torrecillas C, Raso S, Flores ME, et al. Presence and persistence of intestinal parasites in canine fecal material collected from the environment in the province of Chubut, Argentine Patagonia. Vet Parasitol. 2003;117: 263-9.. There are also many reports regarding the environmental pollution in Northeastern Argentina, a subtropical region with high temperatures and high levels of humidity during most of the year. Other noteworthy surveys include those conducted in the city of Corrientes by MILANO et al.1212. Milano AMF, Oscherov EB. Contaminación por parásitos caninos de importancia zoonótica en playas de la ciudad de Corrientes, Argentina. Parasitol Latinoam. 2002;57:119-23.,1313. Milano AMF, Oscherov EB. Contaminación de aceras con enteroparásitos caninos en Corrientes, Argentina. Parasitol Latinoam. 2005;60:82-5. and by ALONSO et al. who evaluated the contamination in Resistencia (Province of Chaco) in 200111. Alonso JM, Stein M, Chamorro MC, Bojanich MV. Contamination of soils with eggs of Toxocara in a subtropical city in Argentina. J Helminthol. 2001;75:165-8. and in 200622. Alonso JM, Luna AC, Fernández GJ, Bojanich MV, Alonso ME. Huevos de Toxocara en suelos urbanos destinados a recreación en una ciudad Argentina. Acta Bioquím Clín Latinoam. 2006;40:219-22..

TABLE 1
Surveys performed on environmental contamination with Toxocara eggs in public locations in Argentina

Contrastingly, there are few reports on soil contamination in rural settlements of the country. However, the reports of CHIODO et al. on the presence of Toxocara spp. eggs in soil samples from General Mansilla, a small rural location in northern Buenos Aires Province55. Chiodo P, Basualdo J, Ciarmela L, Pezzani B, Apezteguía M, Minvielle M. Related factors to human toxocariasis in a rural community of Argentina. Mem Inst Oswaldo Cruz. 2006;101:397-400., and the findings of FILLAUX et al. in some locations in the provinces of Chubut, Neuquén and Río Negro77. Fillaux J, Santillán G, Magnaval JF, Jensen O, Larrieu E, Sobrino-Becaria CD. Epidemiology of toxocariasis in a steppe environment: the Patagonia study. Am J Trop Med Hyg. 2007;76:1144-7. can be cited.

It may be concluded that the negative results found in this work were directly related to the environmental conditions present in the studied area. Temperature is responsible for the rate of embryonation while moisture is essential for encouraging development and maintaining egg viability in general1010. Keegan JD, Holland CV. A comparison of Toxocara canis embryonation under controlled conditions in soil and hair. J Helminthol. 2013;87:78-84.. Regions with high thermal amplitude, low moisture, strong sunlight and soils with little vegetation provide unfavorable conditions for the viability of the eggs of Toxocara spp.

Discovery of eggs in the soil of public areas depends on the presence of canine or feline feces, the hygienic behavior of pet owners, the presence of stray animals without veterinary supervision, weather conditions, laboratory techniques employed in the survey etc, and all these circumstances must be considered when comparing the results found in different geographical regions. Moreover, in order to accurately define the importance of public spaces in the transmission of the infection to humans, it is important to consider the role of backyards or green spaces around housing in small towns, where the population is not used to walking pets in public spaces, and in such cases a significant fraction of the population may acquire the infection within households.

These features justify the need for an international consensus to achieve agreements, in order to standardize methods for soil sampling and laboratory processing, and thus, make results more comparable among the surveys conducted in various regions of the world. This could eventually redefine the epidemiologic importance of public spaces in the transmission of geohelminthic infections to humans.

ACKNOWLEDGEMENTS

To the Secretaría General de Ciencia y Técnica of Univesidad Nacional del Nordeste -Argentina for funding this work, and to Mrs. Mariana Climent for the translation of the manuscript.

REFERENCES

  • 1
    Alonso JM, Stein M, Chamorro MC, Bojanich MV. Contamination of soils with eggs of Toxocara in a subtropical city in Argentina. J Helminthol. 2001;75:165-8.
  • 2
    Alonso JM, Luna AC, Fernández GJ, Bojanich MV, Alonso ME. Huevos de Toxocara en suelos urbanos destinados a recreación en una ciudad Argentina. Acta Bioquím Clín Latinoam. 2006;40:219-22.
  • 3
    Borecka A. Differentiation of Toxocara spp. eggs isolated from the soil by PCR-linked RFLP. Helminthologia. 2004;41:185-7.
  • 4
    Celis Trejo CA, Romero Núñez C, García Contreras AC, Mendoza Barrera GE. Soil contamination by Toxocara spp. eggs in a University in Mexico City. Rev Bras Parasitol Vet. 2012;21:298-300.
  • 5
    Chiodo P, Basualdo J, Ciarmela L, Pezzani B, Apezteguía M, Minvielle M. Related factors to human toxocariasis in a rural community of Argentina. Mem Inst Oswaldo Cruz. 2006;101:397-400.
  • 6
    Córdoba A, Ciarmela ML, Pezzani BC, Gamboa MI, De Luca MM, Minvielle MC, et al. Presencia de parásitos intestinales en paseos públicos urbanos en La Plata Argentina. Parasitol Latinoam. 2002;57:25-9.
  • 7
    Fillaux J, Santillán G, Magnaval JF, Jensen O, Larrieu E, Sobrino-Becaria CD. Epidemiology of toxocariasis in a steppe environment: the Patagonia study. Am J Trop Med Hyg. 2007;76:1144-7.
  • 8
    Fonrouge R, Guardis M, Radman NE, Archelli SM. Contaminación de suelos con huevos de Toxocara sp. en plazas y parques públicos de la ciudad de La Plata, Buenos Aires, Argentina. Bol Chil Parasitol. 2000;55:83-5.
  • 9
    Jacobs DE, Zhu X, Gasser RB, Chilton NB. PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Trop. 1997;68:191-200.
  • 10
    Keegan JD, Holland CV. A comparison of Toxocara canis embryonation under controlled conditions in soil and hair. J Helminthol. 2013;87:78-84.
  • 11
    Martin U, Demonte M. Urban contamination with zoonotic parasites in the central region of Argentina. Medicina (B Aires). 2008;68:363-6.
  • 12
    Milano AMF, Oscherov EB. Contaminación por parásitos caninos de importancia zoonótica en playas de la ciudad de Corrientes, Argentina. Parasitol Latinoam. 2002;57:119-23.
  • 13
    Milano AMF, Oscherov EB. Contaminación de aceras con enteroparásitos caninos en Corrientes, Argentina. Parasitol Latinoam. 2005;60:82-5.
  • 14
    Minvielle MC, Pezzani BC, Basualdo Farjat JA. Frecuencia de hallazgo de huevos de helmintos en materia fecal canina recolectada en lugares públicos de la ciudad de La Plata, Argentina. Bol Chil Parasitol. 1993;48:63-5.
  • 15
    Mizgajska H. Eggs of Toxocara spp. in the environment and their public health implications. J Helminthol. 2001;75:147-51.
  • 16
    National Weather Service. Available from: http://www.smn.gov.ar/
    » http://www.smn.gov.ar/
  • 17
    Quinn R, Smith HV, Bruce RG, Girwood RW. Studies on the incidence of Toxocara and Toxascaris spp. ova in the environment. 1. A comparison of flotation procedures for recovering Toxocara spp. ova from soil. J Hyg (Lond). 1980;84:83-9.
  • 18
    Radman NE, Archelli SM, Fonrouge RD, del V Guardis M, Linzitto OR. Human toxocarosis. It's seroprevalence in the city of La Plata. Mem Inst Oswaldo Cruz. 2000;95:281-5.
  • 19
    Rubel D, Wisnivesky C. Magnitude and distribution of canine fecal contamination and helminth eggs in two areas of different urban structure, greater Buenos Aires, Argentina. Vet Parasitol. 2005;133:339-47.
  • 20
    Sánchez Thevenet P, Jensen O, Mellado I, Torrecillas C, Raso S, Flores ME, et al. Presence and persistence of intestinal parasites in canine fecal material collected from the environment in the province of Chubut, Argentine Patagonia. Vet Parasitol. 2003;117: 263-9.
  • 21
    Santarém VA, Magoti LP, Sichieri TD. Influence of variables on centrifuge-flotation technique for recovery of Toxocara canis eggs from soil. Rev Inst Med Trop Sao Paulo. 2009;51:163-7.
  • 22
    Soriano SV, Pierangeli NB, Roccia I, Bergagna HFJ, Lazzarini LE, Celescinco A, et al. A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquén, Patagonia, Argentina. Vet Parasitol. 2010;167:81-5.
  • 23
    Ybáñez MR, Garijo M, Goyena M, Alonso FD. Improved methods for recovering eggs of Toxocara canis from soil. J Helminthol. 2000;74:349-53.

Publication Dates

  • Publication in this collection
    Jan-Feb 2015

History

  • Received
    16 Oct 2013
  • Accepted
    4 June 2014
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