ABSTRACT

Objective

To evaluate intestinal parasitosis, undernutrition and socio-environmental factors in schoolchildren from Clorinda (Formosa, Argentina).

Materials and Methods

Serial fecal samples and anal swabs of 114 schoolchildren, canine feces and soil samples were analyzed. Body weight and height of 215 schoolchildren were measured and undernutrition was estimated according to the World Health Organization criteria. Socio-environmental variables were assessed by means of a semi-structured questionnaire.

Results

78.1% of children were infected by at least one of the 12 species identified and 70.8% had multiple parasitic infections. Blastocystis sp., Giardia lamblia and Enterobius vermicularis were the most prevalent. Additionally, 17.5% of children were infected by at least one geohelminth (e.g. Ascarislumbricoides, Trichuris trichiura, hookworms). 64.3% of canine of canine feces were positive and six parasitic species were found; the most frequent were Ancylostoma caninum, Uncinaria stenocephala and G. lamblia. Furthermore, 37.5% of soil samples showed zoonotic parasites (i.e. Ascaris sp., Toxocara sp.). Finally, 10.0% of the children were undernourished and 85.7% of them had parasites. The risk for parasitosis was higher in children that lived in houses with inadequate solid waste disposal and whose parents were unemployed or had temporary jobs.

Conclusions

The lack of environmental sanitation, unstable employment of parents and the presence of zoonotic species were the most relevant factors observed. Consequently, these conditions result in an increase of parasitic infections and negatively influence the growth of children.

Key Words:
Parasites; malnutrition; environment; children (source: MeSH, NLM)

RESUMEN

Objetivo

Evaluar la parasitosis intestinal, la desnutrición y los factores socio-ambientales en escolares de Clorinda (Formosa, Argentina).

Materiales y Métodos

Se analizaron muestras fecales y escobillados anales seriados de 114 escolares, heces caninas y muestras de suelo. Se midió el peso corporal y la talla de 215 escolares y se evaluó la desnutrición según los criterios de la Organización Mundial de la Salud. Las variables socio-ambientales se evaluaron mediante una encuesta semiestructurada.

Resultados

El 78,1% de los niños estuvieron parasitados por al menos 1 de las 12 especies identificadas y el 70,8% presentó parasitosis múltiples. Blastocystis sp., Giardia lamblia y Enterobius vermicularis fueron las más prevalentes. Además, el 17,5% de los niños estaban infectados con al menos un geohelminto (e.g. Ascaris lumbricoides, Trichuris trichiura, ancylostomideos). El 64,3% de las heces caninas resultaron positivas y se encontraron seis especies parasitarias; las más frecuentes fueron Ancylostoma caninum, Uncinaria stenocephala y G. lamblia. Además, el 37,5% de las muestras de suelo mostraron parásitos zoonóticos (i.e. Ascaris sp., Toxocara sp.). Finalmente, el 10% de los niños estaban desnutridos y el 85,7% de ellos resultaron parasitados. El riesgo de parasitosis fue mayor en los niños que vivían en casas con eliminación inadecuada de desechos sólidos y cuyos padres estaban desempleados o tenían empleos temporales.

Conclusiones

La falta de saneamiento ambiental, el empleo inestable de los padres y la presencia de especies zoo-nóticas fueron los factores observados más relevantes. En consecuencia, estas condiciones resultan en un aumento de las infecciones parasitarias e influyen negativamente en el crecimiento de los niños.

Palabras Clave:
Parásitos; malnutrición; ambiente; niños (fuente: DeCS, BIREME)

Intestinal parasitosis is a neglected infectious disease that is found worldwide. This disease is highly prevalent in tropical and subtropical areas of low-income developing countries. ¹1. Organización Panamericana de la Salud. Reunión regional para intensificar los esfuerzos de control de la Helmintiasis transmitidas por contacto con el suelo, o geohelmintiasis en las Américas. (Lima, 1-3 agosto 2016). Washington, D.C.: OPS; 2017. Available from: http://bit.ly/37IPNjA.
http://bit.ly/37IPNjA... Recent estimates are that more than one billion people of developing regions of Africa, Asia and America are infected by parasitic helminth species, of which more than 1 450 million are infected by at least a species of intestinal nematode; this number could be higher if pathogenic intestinal protozoa were considered. ²2. Lustigman S, Prichard RK, Gazzinelli A, Grant WN, Boatin BA, McCarthy JS, et al. A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Negl Trop Dis. 2012; 6: e1582.^,33. Juárez M, Rajal V. Parasitosis intestinales en Argentina: principales agentes causales encontrados en la población y en el ambiente. Rev Argent Microbiol. 2013; 45(3): 191-204. Even if these parasitic infections do not lead to immediate death, they may have negative effects on the physical and cognitive development of children, such as malabsorption syndrome, anemia, anorexia, chronic inflammation, undernutrition and diarrhea. ⁴4. Cabada MM, Goodrich MR, Graham B, Villanueva-Meyer PG, Deichsel EL, Lopez M, et al. Prevalence of intestinal helminths, anemia, and malnutrition in Paucartambo, Peru. Rev Panam Salud Publica. 2015; 37(2): 69-75.^,55. Duedu K, Peprah E, Anim-Baidoo I, Ayeh-Kumi P. Prevalence of intestinal Parasites and association with malnutrition at a Ghanaian Orphanage. Human Parasitic Diseases. 2015; 7: 5-9..

The constant growth of the population and urbanization, the increase of migrations, the lack of sanitary facilities, inadequate hygiene and limited access to health services favor the transmission of parasites, and the consequent infections ⁶6. Norman F, Monge-Maillo B, Martínez-Pérez Á, Perez-Molina J, López-Vélez R. Parasitic infections in travelers and immigrants: part II helminths and ectoparasites. Future Microbiol. 2015; 10(1): 87-99.. In this sense, parasitosis can be caused by the ingestion of infecting cysts or eggs present in the soil, water and raw food, or by the penetration of larvae from the soil through the skin. ³3. Juárez M, Rajal V. Parasitosis intestinales en Argentina: principales agentes causales encontrados en la población y en el ambiente. Rev Argent Microbiol. 2013; 45(3): 191-204. Biological contamination of the environment with pet feces is also a serious problem for public health, since their parasitic forms can infect humans as well. One example is visceral larva migrans and ocular larva migrans caused by Toxocara sp., and cutaneous larva migrans caused by Ancylostoma caninum, A. brasiliense, and Uncinaria stenocephala⁷7. Armstrong WA, Oberg C, Orellana JJ. Presencia de huevos de parásitos con potencial zoonótico en parques y plazas públicas de la ciudad de Temuco, Región de La Araucanía, Chile. Arch Med Vet. 2011; 43(2): 127-134..

In Argentina, a country with a wide geographical and climatic diversity, the prevalence of intestinal parasitosis shows a declining trend from north to south and from east to west that accounts for the complex mosaic of social, economic, and environmental variability of its territory. ⁸8. Navone GT, Zonta ML, Cociancic P, Garraza M, Gamboa MI, Giambelluca LA, et al. Estudio transversal de las parasitosis intestinales en poblaciones infantiles de Argentina. Rev Panam Salud Pública. 2017; 41: e24. In this context, the north of the country presents socio-economic and environmental conditions that favor the development of these infections. Since information about these infections in north-eastern Argentina is scarce, the aim of this study was to evaluate intestinal parasitosis, undernutrition and socio-environmental factors in schoolchildren from Clorinda (Formosa, Argentina).

MATERIALS AND METHODS

Population and study area

The study was carried out in children of both sexes from school No. 372 in Clorinda. The school has 350 primary school students coming from peripheral neighborhoods.

Clorinda (in the department of Pilcomayo, province of Formosa) (25°17'S, 57°43'W) is a city located in the north-east of Argentina bordering Paraguay (Figure 1). The climate of the area is subtropical with an average annual temperature of 24°C, a marked seasonal variation and annual rainfall that can exceed 1 200 mm. Soils are clay-slime with poor to imperfect drainage.

A cross-sectional study was carried out in September 2014. The selection of the sample was non-probabilistic and largely determined by voluntary participation.

This study included children who had not received antiparasitic treatment at the time of the research and whose parents or legal guardians signed an informed consent. Children with no parental or guardian consent and with chronic diseases or pathological conditions were excluded.

Parasitological study

Meetings with adults and children were initially held to inform them about the biology and strategies to prevent intestinal parasites and aspects related to the nutritional status of children. Free parasitology tests for children and dogs were offered. Every consenting family was provided with one vial per dog and two vials per child of formalin 10% for stool samples, and anal swabs to diagnose intestinal parasites.

The study included 114 children (51.8% boys and 48.2% girls) aged 1-14 and divided into 3 age groups (1.0-5.9, 6.09.9 and 10.0-14.9). Fecal and anal swab samples of children were collected by their parents or legal guardians during 5-7 days. Anal swabs were obtained from the perianal zone during the morning using sterile gauze. Feces from dogs (n=16) were collected during 3-5 days by their owners or by the research group immediately after deposition.

Coproparasitological samples were processed using concentration by sedimentation (Ritchie) and flotation (Willis) techniques. Anal swab vials were agitated vigorously and centrifuged for 10 minutes at 400g (gravity) to obtain a pellet with the highest possible concentration of eggs of Enterobius vermicularis⁹9. World Health Organization. Medios auxiliares para el diagnóstico de las parasitosis intestinales. World Health Organization: Geneva, 1994.^,1010. Girard de Kaminsky R. Manual de parasitología: técnicas para laboratorios de atención primaria de salud y para el diagnóstico de las Enfermedades Infecciosas Desatendidas. 3era ed. Honduras: Organización Panamericana de la Salud; 2014..

Soil samples (n=16) were collected from the perido-miciliary area of the participating families using a grid of 20x20cm and 5cm depth. They were processed applying the decantation and centrifugation technique of Shurtleff & Averre ¹¹11. Shurtleff MC, Averre CW. Diagnosing plant diseases caused by nematodes. Chapter 2 Methods. Extracting Nematodes from Plant Tissue or Soil. Centrifugal flotation. St Paul, Minnesota: American Phytopathological Societ Press; 2000. p 37-38.13..

Every sample was examined by experts using an optical microscope at 100X and 400X magnification, and eggs, cysts and larvae were identified based on their measures and morphological characteristics ⁹9. World Health Organization. Medios auxiliares para el diagnóstico de las parasitosis intestinales. World Health Organization: Geneva, 1994.^,1212. Chaves EJ, Echeverría MM, Torres M. Clave para determinar géneros de nematodos del suelo de la República Argentina. Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Mar del Plata; 1995. pp. 91..

Anthropometric study

The study included 215 children (55.8% boys and 44.2% girls) aged 6-12 divided into 2 age groups (6.0-9.9 and 10.0-12.9). A single technician performed anthropometric measurements according to standard protocols. ¹³13. Lohman TG, Roche AF, Martorell R. Anthropometric standardization reference manual. Illinois: Human Kinetics Books; 1988. Age, body weight and height were recorded: age was obtained from identification cards or school records, body weight was measured in kilograms (kg) using a digital scale (Tanita UM-061, 100g accuracy) with children lightly dressed (to correct for clothing, the weight of clothes was subtracted), and height was measured in centimeters (cm) using a portable vertical anthropometer (SECA, 1 mm accuracy).

The exact age of each child was calculated as a function of their birth date. Similarly, body mass index [BMI = (W/H²) (kg/m²)] was estimated according to weight and height data. Underweight (low weight-for-age, LW/A), stunting (low height-for-age, LH/A) and low BMI-for-age (LBMI/A) were determined using the World Health Organization (WHO) reference charts and -2 Z scores as cut-off points ¹⁴14. World Health Organization. Multicentre growth reference study group. WHO Child growth standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. World Health Organization: Ginebra; 2006..

Socio-environmental study

A semi-structured questionnaire was completed by the parents or legal guardians (n=113) to evaluate the socio-environmental characteristics with information regarding structural and physical facilities. These characteristics provided information about indoor and outdoor housing conditions. Moreover, parents' educational level, employment, governmental food and monetary support, hygiene and cultural practices were considered, among others ¹⁵15. Oyhenart EE, Castro LE, Forte LM, Sicre ML, Quintero FA, Luis MA, et al. Socioenvironmental conditions and nutritional status in urban and rural schoolchildren. Am J Hum Biol. 2008; 20(4): 399-405.

16. Zonta ML, Oyhenart EE, Navone GT. Socio-environmental variables associated to malnutrition and intestinal parasitoses in the child population of Misiones, Argentina. Am J Hum Biol. 2014; 26: 609-16.^-1717. Cociancic P, Zonta ML, Navone GT. A cross-sectional study of intestinal parasitoses in dogs and children of the periurban area of La Plata (Buenos Aires, Argentina): Zoonotic importance and implications in public health. Zoonoses and Public Health. 2017; 65: e44-e53..

Statistical analysis

Data were analyzed by software R ¹⁸18. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: http://www.R-project.org/2015.
http://www.R-project.org/2015... . Parasitosis and parasitic species were analyzed in relation to sex and age group, socio-environmental characteristics, hygiene practices and nutritional status. The independence of the variables was evaluated using the Chi square test (x²) or Fisher's exact test at a significance level of p<0.05. Socio-environmental variables were examined by means of logistic regression models with a stepwise forward selection to determine risk factors for parasitic infection in children. The model with the lowest residual deviance was chosen and, in case of several competitive models, the most parsimonious was selected comparing Akaike information criterion and p-value. Association force was estimated by odds ratio (OR) values. Level of significance p<0.05 and confidence intervals (CI) were used. To perform a regression analysis, the educational level of parents was grouped into unschooled/primary (basic education) and secondary/tertiary/university (higher education); employment status was divided into unemployed/ temporary and permanent/freelance.

Ethics statement

The study was carried out without affecting the physical, psychic and moral inte Blastocystis grity of the participants and protecting their privacy. The principles proclaimed in the Universal Declaration of Human Rights (1948), the ethical standards established by the Nüremberg Code (1947), the Declaration of Helsinki (1964) and its successive amendments were taken into consideration. Special attention was also paid to Article 5 of the Regulation Decree of National Law 25.326.

All families involved were given the results of the para-sitology diagnosis, and positive cases were referred to the nearest healthcare center and to the school to receive the corresponding antiparasitic treatment.

RESULTS

Parasitological analysis in children

Of the total number of analyzed children, 78.1% (89/114) were infected with at least one intestinal parasite species. Infection was slightly more frequent in boys than in girls (51.7% vs. 48.3%; p>0.05), as well as in 6.0-9.9 year-old children (58.4%) with respect to younger and older children (18.0% and 23.6%, respectively; p>0.05).

Twelve parasitic species were identified. Infection by pathogenic species was higher than infection by non-pathogenic species (76.3% vs. 1.8%), and the most prevalent were Blastocystis sp. (57.9%), Giardia lamblia (36.8%) and E. vermicularis (19.3%). Entamoeba coli were the most prevalent (21.1%) of the non-pathogenic protozoa. In addition, 17.5% (20/114) were positive for some species of geohelminth, and the most frequent were Ascaris lumbricoides and Trichuris trichiura (7.9% and 7.0, respectively) (Table 1).

Multiple parasite infections (children infected by two or more species) were more frequent than monoparasitosis (children infected by a single species) (70.8% vs. 29.2%; p>0.05), observing a maximum of 5 species in some cases. Multiple infections were more prevalent in girls than in boys (37.1% vs. 33.7%; p>0.05) and in children between 6.0-9.9 years of age (40.4%) with respect to younger and older children (12.3% and 17.9%, respectively; p>0.05).

Statistically significant associations were observed between Blastocystis sp./G. lamblia (x²=4.2, p<0.05); Blastocystis sp./E. coli (x²=4.6, p<0.05); G. lamblia/E. coli (x²=4.9, p<0.05); and E. vermicularis/A. lumbricoides (Fisher= 0.01).

Parasitological analysis in dogs and soil

Of the total number of analyzed dogs, 68.7% (11/16) were infected with at least one species. Six species were identified and all of them were pathogenic. The most prevalent nematodes were A. caninum (62.5%) and U. stenocephala (37.5%), followed by Dioctophymarenale and Aelurostrongylus abstrusus (6.2%). Among the protozoa found, 25% of the samples were positive for G. lamblia. As for cestodes, eggs of Spirometra spp. were identified (12.5%).

Regarding the soil samples collected, 81.2% were positive (13/16) for at least some parasitic form: 37.5% showed parasites of zoonotic importance (i.e. Ascaris sp., Toxocara sp.), and 18.7% revealed eggs of veterinary importance (i.e. Bunostomum sp., Cooperia sp., Ostertagia sp.).

Anthropometric analysis

Of all children measured anthropometrically, 60.9% (131/215) were well-nourished and 10.2% (22/215) were undernourished.

The analysis of undernutrition revealed that 3.5% were underweight, 0.9% had low BMI-for-age, and 9.3% presented stunted growth. Age group and sex comparisons showed no significant differences (p>0.05) (Table 2).

Seventy-four children were anthropometrically and parasitologically evaluated and 9.5% (7/74) of them showed some type of undernutrition. Undernourished children had more parasitic infections than well-nourished children (85.7% vs. 51.3%) and they were also more infected by Blastocystis sp. (85.7% vs. 51.0%) and A. lumbricoides (14.3% vs. 8.2%). The percentages of infection by G. lamblia in well-nourished and undernourished children were similar (30.6% and 28.6%, respectively).

Socio-environmental analysis

Most families owned the houses they lived in, which were mainly made of brick masonry, and had concrete floors and access to piped water. However, most of them had septic tanks and latrines for wastewater disposal. Domestic solid waste was usually burnt for there was no public collection. Most roads were made of dirt and houses flooded frequently. The majority of the participants lived in overcrowded conditions and shared single beds (Table 3).

With respect to the educational attainment of parents, the majority of them had only completed primary education. As for their employment status, 38.1% of fathers had temporary jobs and mothers were mostly unemployed or were housewives (44.2%) (Table 3).

The families received monetary and food support from the government (49.6% and 10.6%, respectively) and most of them had access to the public health system. Besides, most families owned pets and only a few practiced animal husbandry and orchard agriculture for personal consumption (Table 3).

As for hygiene practices, most adults stated that their children always washed their hands before eating (76.1%) and after going to the toilet (73.5%) and playing with their pets (58.4%). Additionally, they claimed that they washed fruits and raw vegetables before consumption (76.1%).

About cultural practices, 71.7% of children usually walked barefoot, 46.9% had onychophagia, and 79.6% played in the soil.

The risk of parasitic infection was higher in children that lived in houses where the disposal of domestic residues was inadequate (OR=4.4, 95% CI 1.4-13.7). The analysis of each parasitic species showed that the risk of infection by Blastocystis sp. and G. lamblia was greater in children whose parents were unemployed or had temporary jobs (OR=3.8, 95% CI 1.04-13.9 and or=15.7, 95% CI = 1.6-154.4, respectively). Furthermore, the risk of infection by G. lamblia was high in families that received no monetary support from the government (OR=4.7, 95% CI = 1.2-18.3).

DISCUSSION

Of the total number of analyzed children, 78.1% were infected by at least one of the 12 parasite species identified, result that reveals disparity when compared with other populations. In this regard, studies in Venezuela and Paraguay reported a lower prevalence (63% and 35%, respectively) ¹⁹19. Devera R, Blanco Y, Amaya I. Prevalencia de parásitos intestinales en escolares de Ciudad Bolívar, Venezuela: comparación de dos períodos. Kasmera. 2015; 43(2): 122-9.^,2020. Echagüe G, Sosa L, Díaz V, Ruiz I, Rivas L, Granado D et al. Enteroparasitosis en niños bajo 5 años de edad, indígenas y no indígenas, de comunidades rurales del Paraguay. Rev Chilena Infectol. 2015; 32(6): 649-657., but similar or slightly higher prevalence in studies performed in other Latin American countries. ²¹21. Cañete R, Díaz MM, Avalos García R, Laúd Martinez PM, Manuel Ponce F. Intestinal parasites in children from a Day Care Centre in Matanzas City, Cuba. PLoS ONE. 2012; 7: e51394.^,2222. Abreu dos Santos A, Gurgel-Gonçalves R, Rodrigues Machado E. Factors associated with the occurrence of intestinal parasites in children living in the Federal District of Brazil. Rev Patol Trop. 2014; 43: 89-97. In Argentina, prevalence was not uniform either since the distribution of parasitic infections changed according to region: values were over 80% in the north ¹⁶16. Zonta ML, Oyhenart EE, Navone GT. Socio-environmental variables associated to malnutrition and intestinal parasitoses in the child population of Misiones, Argentina. Am J Hum Biol. 2014; 26: 609-16.^,2323. Dib J, Oquilla J, Lazarte SG, González SN. Parasitic prevalence in a suburban school of Famaillá, Tucumán, Argentina. ISRN Microbiol. 2012; 1-4., between 60% and 70% in the center ²⁴24. Gamboa MI, Giambelluca LA, Navone GT. Distribución especial de las parasitosis intestinales en la ciudad de La Plata, Argentina. Medicina (B Aires). 2014; 74: 363-370.^,2525. Garraza M, Zonta ML, Oyhenart EE, Navone GT. Estado nutricional, composición corporal y enteroparasitosis en escolares del departamento de San Rafael, Mendoza, Argentina. Nutr Clin Diet Hosp. 2014; 34(1): 31-40., and lower than 40% in the south ⁸8. Navone GT, Zonta ML, Cociancic P, Garraza M, Gamboa MI, Giambelluca LA, et al. Estudio transversal de las parasitosis intestinales en poblaciones infantiles de Argentina. Rev Panam Salud Pública. 2017; 41: e24..

In this study, boys turned out to be slightly more infected than girls, as well as children aged 6-9 years with respect to younger and older children. Moreover, and in agreement with other studies, no statistically significant association among the variables sex and age was found. ¹⁹19. Devera R, Blanco Y, Amaya I. Prevalencia de parásitos intestinales en escolares de Ciudad Bolívar, Venezuela: comparación de dos períodos. Kasmera. 2015; 43(2): 122-9.^,2626. Molina N, Pezzani B, Ciarmela M, Orden A, Rosa D, Apezteguía M, et al. Intestinal parasites and genotypes of Giardia intestinalis in schoolchildren from Berisso, Argentina. J Infect Dev Ctries. 2011; 5 (7): 527-34. Despite this, the results suggested that school-age children were the most affected by intestinal parasitosis probably because they had not yet consolidated certain hygiene habits and/ or had greater contact with the sources of infection ²⁷27. Calchi La Corte M, Rivero de Rodríguez Z, Bracho Mora A, Villalobos R, Acurero de Yamarte E, Maldonado A et al. Prevalencia de Blastocystis sp. y otros protozoarios comensales en individuos de Santa Rosa de Agua, Maracaibo, estado Zulia. Rev Soc Venez Microbiol. 2013; 33: 66-71..

Furthermore, 76.3% of the children included in this study were infected by pathogenic species, being Blastocys-tis sp. and G. lamblia the most prevalent protozoa, which are species also considered the most frequent by other researchers ¹⁹19. Devera R, Blanco Y, Amaya I. Prevalencia de parásitos intestinales en escolares de Ciudad Bolívar, Venezuela: comparación de dos períodos. Kasmera. 2015; 43(2): 122-9.^,2828. Liao C, Chuang T, Huang Y, Chou C, Chiang C, Lee F et al. Intestinal parasitic infections: Current prevalence and risk factors among schoolchildren in capital area of the Republic of Marshall Islands. Acta Trop. 2017; 176: 242-248.. Among the non-pathogenic species, E. coli showed the highest value; this type of protozoa associated significantly as they share the same way of transmission in water, soil and food when contaminated with feces ³3. Juárez M, Rajal V. Parasitosis intestinales en Argentina: principales agentes causales encontrados en la población y en el ambiente. Rev Argent Microbiol. 2013; 45(3): 191-204.^,2828. Liao C, Chuang T, Huang Y, Chou C, Chiang C, Lee F et al. Intestinal parasitic infections: Current prevalence and risk factors among schoolchildren in capital area of the Republic of Marshall Islands. Acta Trop. 2017; 176: 242-248.. In this context, it should be noted that most of the population studied used septic tanks and latrines or practiced open defecation, and that most houses flooded frequently, favoring the dispersion of these parasites.

Among nematodes, E. vermicularis was the most frequently found. Enterobius vermicularis infection is favored by gaming habits and personal hygiene practices of children, as well as by bed-sharing and overcrowding. ²⁹29. Li H, Zhou C, Li Z, Deng Z, Ruan C, Zhang Q et al. Risk factors for Enterobius vermicularis infection in children in Gaozhou, Guangdong, China. Infect Dis Poverty. 2015; 4(1): 28. As for the population studied, 50% lived in overcrowded conditions and shared single beds. Moreover, 47% of children had onychophagia.

As for geohelminth infection, 17.5% of children were positive for at least one geohelminth species with values that fluctuated between 0.9-7.9%. In this regard, the presence of these species is favored by warm and humid climate and abundant rainfall, as well as by deficient sanitary conditions such as inadequate excreta disposal, lack of drinking water and floods, all of which characterize and are common in Clorinda. In addition, the lack of access to information and a deficient nutritional status might increase the risk of infection by geohelminths ³⁰30. Kaminsky RG, Ault SK, Castillo P, Serrano K, Troya G. High prevalence of soil-transmitted helminths in Southern Belize-highlighting opportunity for control interventions. Asian Pac J Trop Biomed. 2014; 4(5): 345-353.^,3131. Alelign T, Degarege A, Erko B. Soil-Transmitted helminth infections and associated risk factors among schoolchildren in Durbete Town, Northwestern Ethiopia. J Parasitol Res. 2015; 2015: 1-5. The presence of this helminths may also be related to the behavior of vulnerable populations whose hygienic and cultural practices, such as walking barefoot or not washing their hands, are relevant ³²32. Gamboa MI, Zonta ML, Navone GT. La prevalencia de geohelmintiasis se relaciona con las condiciones socioambientales. Salud Cienc. 2012; 19(1): 16-21.. Consequently, infection by geohelminth species in this study was not surprising after finding that more than 75% of children went around barefoot and played in the soil.

This research showed that 70.8% of the analyzed schoolchildren had multiple parasitic infections and the most frequent associations were among protozoa that are transmitted in a similar way (Blastocystis sp., G. lamblia and E. coli). It has been reported that multiple intestinal infections in children is a widespread phenomenon caused by the interaction of common environmental factors, means of infection, host exposure, susceptibility, as well as behavioral and socio-economic factors that facilitate the co-occurrence of diverse parasites ³³33. Fernández-Niño JA, Astudillo-García CI, Segura LM, Gómez N, Salazar AS, Tabares JH et al. Perfiles de poliparasitismo intestinal en una comunidad de la Amazonia colombiana. Biomédica. 2017; 37(3): 368-377..

About the analyzed dogs, 68.7% were infected, being A. caninum, U. stenocephala and Giardia sp. the most prevalent species. In addition, a small percentage of D. renale and Spirometra sp., as well as larvae of A. abstrusus, was identified. The finding of D. renale in feces was unusual; however, their presence could have been caused by cross-contamination with urine. Spirometra is a genus of pseudophyllid cestodes that infects canines and felines, but causes sparganosis in humans by either drinking water contaminated with infected copepods (intermediate host) or by consuming raw meat of infected second intermediate hosts or paratenic hosts (including fish, reptiles and amphibians) ³⁴34. Petrigh RS, Scioscia NP, Denegri GM, Fugassa MH. Cox-1 gene sequence of Spirometra in Pampas foxes from Argentina. Helminthologia. 2015; 52(4): 355-9.. Aelurostrongylus abstrusus is a strongylid nematode that affects the respiratory system of domestic cats and other wild felids, which acquire the infection by ingesting infective larvae encysted with paratenic hosts (usually snails or birds) ³⁵35. Giannelli A, Capelli G, Joachim A, Hinney B, Losson B, Kirkova Z et al. Lungworms and gastrointestinal parasites of domestic cats: a European perspective. Int J Parasitol. 2017; 47:517-528.. In this context, Spirometra sp. and A. abstrusus have been reported for the first time in Clorinda. Most of the species found in dogs were potentially zoonotic and, therefore, able to affect human health. This study also showed the presence of eggs of Ascaris sp. and Toxocara sp. in the soil. These results confirm that the presence of zoonotic species is favored by inadequate disposition canine feces, the lack of environmental sanitation, a close contact with pets, and, eventually, the presence of intermediate hosts essential to complete the life cycle of some parasitic species (i.e. D. renale, Spirometra sp. and A. abstrusus)¹⁷17. Cociancic P, Zonta ML, Navone GT. A cross-sectional study of intestinal parasitoses in dogs and children of the periurban area of La Plata (Buenos Aires, Argentina): Zoonotic importance and implications in public health. Zoonoses and Public Health. 2017; 65: e44-e53.^,3434. Petrigh RS, Scioscia NP, Denegri GM, Fugassa MH. Cox-1 gene sequence of Spirometra in Pampas foxes from Argentina. Helminthologia. 2015; 52(4): 355-9.^,3636. Valente R, Diaz JI, Salomon OD, Navone GT. Natural infection of the feline lungworm Aelurostrongylus abstrusus in the invasive snail Achatina fulica from Argentina. Veterinary Parasitology. 2017; 235: 17-19..

The prevalence of undernutrition (10.2%) was high compared to other provinces of Argentina. ³⁷37. Garraza M, Cesani M, Navone G, Oyhenart E. Malnutrition and body composition in urban and rural schoolchildren: A cross-sectional study in San Rafael, Mendoza (Argentina). Am J Hum Biol. 2016; 28(6): 796-803.^,3838. Navazo B, Dahinten SL, Oyhenart EE. Malnutrición y pobreza estructural. Comparación de dos cohortes de escolares de Puerto Madryn, Argentina. Rev Salud Pública (Bogotá). 2018; 20(1): 60-66. Moreover, prevalence of underweight (3.5%) and stunting (9.3%) showed that children experience serious nutritional deficiencies as a consequence of the limited socio-economic conditions of their families, inadequate hygiene practices and sanitation. This scenario was reflected in undernourished children who were the most infected, especially by Blastocystis sp. and A. lumbricoides. Other studies also confirmed an association between malnutrition and parasitism, and stated that it could be due to the negative effect that enteroparasites have on the physical and cognitive development of children, or by the effect of the nutritional deficit on the immune response, which in turn increases the chances of acquiring parasitic infections ⁵5. Duedu K, Peprah E, Anim-Baidoo I, Ayeh-Kumi P. Prevalence of intestinal Parasites and association with malnutrition at a Ghanaian Orphanage. Human Parasitic Diseases. 2015; 7: 5-9.^,3939. Orden A, Apezteguía M, Ciarmela M, Molina N, Pezzani B, Rosa D et al. Nutritional status in parasitized and nonparasitized children from two districts of Buenos Aires, Argentina. Am J Hum Biol. 2014; 26(1): 73-9..

Lastly, the regression analysis showed that the risk of being infected was higher in children who lived in houses where the disposal of domestic residues was inadequate and whose parents were unemployed or had temporary jobs. Other researches demonstrated that access to housing with basic sanitary services (e.g. drinking water, adequate excreta and solid waste disposal) and having educated and employed parents have a direct impact on the health of children ⁴⁰40. Alvarado BE, Vásquez LR. Determinantes sociales, prácticas de alimentación y consecuencias nutricionales del parasitismo intestinal en niños de 7 a 18 meses de edad en Guapi, Cauca. Biomedica. 2006; 26(1): 81..

The results show that the lack of environmental sanitation, unstable employment of parents and the presence of zoonotic species were the most relevant factors in the analyzed population. Consequently, these conditions result in an increase of parasitic infections and influence the growth of children negatively. This study aims at increasing the parasitological knowledge of the region to improve the nutritional status of children and the sanitation of the environment through a comprehensive approach to prevent and control intestinal parasitosis.

Acknowledgement: The authors would like to thank the local authorities, the education community and the people living in the surveyed neighborhoods for their active cooperation. We are also thankful to Graciela Minardi for her help with the statistical analyses, to Macarena Zarza for her support with the laboratory tests, and to Pilar Martínez for revising and proof reading the manuscript•

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