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Revista Peruana de Medicina Experimental y Salud Publica

versão impressa ISSN 1726-4634versão On-line ISSN 1726-4642

Rev. perú. med. exp. salud publica vol.40 no.4 Lima out./dic. 2023  Epub 18-Dez-2023

http://dx.doi.org/10.17843/rpmesp.2023.404.12984 

Brief report

Prevalence of intestinal parasites in children and domestic animals from two peri-urban neighborhoods in northeastern Argentina

Rumesilda E. Alegre1  , Licentiate in Biological Sciences
http://orcid.org/0000-0003-2171-2501

María de los Ángeles Gómez-Muñoz1  , PhD in Biology
http://orcid.org/0000-0003-2083-8858

Esteban J. Flores-Lacsi1  , Biological Sciences Undergraduate Student
http://orcid.org/0009-0009-6427-408X

María del Rosario Robles2  , PhD in Natural Sciences
http://orcid.org/0000-0003-4197-8040

Francisca Milano1  , PhD in Natural Sciences
http://orcid.org/0009-0006-3502-8910

1 Laboratory of Parasite Biology, BioVyP Research Group. Faculty of Exact and Natural Sciences and Surveying., Universidad Nacional del Nordeste, Corrientes, Argentina.

2 Center for Parasitological and Vector Studies (CEPAVE-CONICET-UNLP), La Plata, Buenos Aires, Argentina.

ABSTRACT

This study aimed to examine the prevalence of intestinal parasites in children and domestic animals from two peri-urban neighborhoods in Corrientes, Argentina. We also evaluated the characteristics of humans, socio-environmental features, and hygiene practices associated with the presence of parasites. Fecal samples were examined using techniques of concentration by sedimentation and flotation. The Graham method was used to diagnose Enterobius vermicularis eggs in children. We carried out the univariate and bivariate analysis of the data. We analyzed 58 dwellings, from which we obtained 146 stool samples from children and 101 from animals. We found at least one parasite species in 54 dwellings (93.1%). We found that 52.7% of children had parasites, mainly Blastocystis spp. (35.6%) and Giardia spp. (21.2%). We found that 67.32% of the animals had parasites, the most prevalent species being hookworms (60.7%). In conclusion, it is evident that the domestic environment can favor the transmission of these parasites.

Keywords: Child; domestic animals; parasitic intestinal diseases; prevalence; zoonoses; Argentina

KEY MESSAGES

Motivation for the study. There are few reports on intestinal parasites in children and domestic animals in urban areas in Argentina who live in homes with characteristics that favor the maintenance and transmission of parasites of zoonotic importance.

Main findings. More than 50% of children and pets were parasitized, most of them with zoonotic pathogens.

Implications. Our results showed the urgent need to improve sanitary control of children and animals, and to implement activities for the prevention of intestinal parasitosis in the homes analyzed.

Keywords: Child; domestic animals; parasitic intestinal diseases; prevalence; zoonoses; Argentina

INTRODUCTION

Endoparasites of humans and domestic animals can multiply under favorable conditions, and can be transmitted among the inhabitants of the house 1,2. These favorable conditions are commonly associated to factors related to the individual (age, sex, nutritional status, etc.) 3, and/or socio-environmental risk factors such as the inadequate disposition of stool, unsuitable personal hygiene habits, and unequal access to education and health, among others 4.

In this regard, the number of slums has increased in Argentina, which lack basic services such as drinking water, electricity and adequate sanitation 5. The overall prevalence rates of endoparasites in Argentinean children and their pets have been reported to be 64.8% and 85.7% and 8.9% and 41%, respectively 6,7,8.

Specifically, 3.6% of dwellings in the province of Corrientes are not adequate for living, 6.5% lack basic sanitary conditions, 11.0% are critically overcrowded, and 37% are located in vulnerable areas (near garbage dumps or flood-prone land) 9. However, few parasitological studies have taken these variables into account 10.

Therefore, we consider that the city of Corrientes, in northeastern Argentina, could represent a high-risk area for the transmission and maintenance of potentially zoonotic parasites. We also identified important gaps in parasitology research involving human, animal and environmental factors, i.e. operating under the One Health approach, which hinders the interpretation of all these factors together, as well as the opportunity to propose control and prevention measures.

This study aimed to examine the prevalence of intestinal parasites in children and domestic animals in two periurban neighborhoods of the Capital Department (Corrientes, Argentina). In addition, some human characteristics (sex and age), socio-environmental traits and hygiene practices were evaluated as possible risk factors for parasitic infection.

THE STUDY

Study design

We conducted a cross-sectional, observational, descriptive study. The population was contacted between 2018 and 2021 in an elementary school. The sample size was not calculated; we included all households whose inhabitants agreed to participate. The unit of analysis was the dwelling 2.

Study area

The study was conducted in two suburban neighborhoods (A and B) of the Capital Department of Corrientes Province (27°28'00" S, 58°50'00" W), northeastern Argentina (Figure 1). These neighborhoods are characterized by poor sanitary conditions and a high degree of contact with domestic and synanthropic animals, among others.

Figure 1 Geographical location of the Province of Corrientes in northeastern Argentina (a), Capital Department (b) and the peri-urban neighborhoods analyzed (c). 

Sample collection

A collection kit for each child and pet were delivered to every home. The kit consisted of stool collection bottles with 10% formaldehyde and Graham’s test for the diagnosis of intestinal parasites. Verbal explanations were provided to the participants, which were supplemented by illustrated instructions included in the kit. Children of both sexes aged 0 to 14 years participated in the study. Participants were divided into two age groups: out-of-school children (aged 3 years or less) and school children (aged 4 years or more). Stool and perianal mucosa samples were collected by parents for 5-6 consecutive days. Stool samples from the animals were collected by their owners for 3-4 consecutive days or by the research team. Owners were advised to collect fecal samples from the animals immediately after the animals defecate and in a central area to avoid possible contamination.

Socio-environmental and demographic data collection

Data were collected through direct observation of the family environment and the application of questionnaires. Data were related to different risk variables or exposure factors, including hygiene practices (Tables 1 and 2).

Table 1 Socio-environmental characteristics of the population in the peri-urban neighborhoods analyzed in the city of Corrientes. 

Characteristics n (%) a
Overcrowding (persons per room)
Yes 28 (50)
No 28 (50)
Presence of domestic animals
Yes 52 (92.9)
No 4 (7.1)
Floor type (inside the house)
Cement or other 49 (87.5)
Sand/earth 7 (12.5)
Floor type (outside the house)
Cement or other 4 (7.1)
Sand/earth 52 (92.9)
Main water source
Well 17 (30.3)
Community water network (potable) 39 (69.7)
Disposal of human feces
Latrine 34 (60.8)
Installed bathroom 22 (39.2)
Flood risk
Never 37 (66.1)
Occasionally 19 (33.9)
Disposal of animal feces
Stays on the ground 21 (37.5)
Disposed of in bags 35 (62.5)
Wastewater disposal
Cesspool 55 (98.2)
Outdoor 1 (1.8)
Solid waste disposal
Collected by the municipality 29 (51.8)
Open air or incineration 27 (48.2)
Disposal of diapers
Collected by the municipality 23 (41.1)
Open air or incineration 23 (41.1)
Do not use diapers 10 (17.8)
Presence of rodents
Yes 6 (10.8)
No 46 (82.1)
No data 4 (7.1)
Antiparasitic drug treatment in humans
Yes 15 (26.8)
No 41 (73.2)
Pharmacological antiparasitic treatment in animals
Yes 3 (5.3)
No 53 (94.7)
Mother’s education
Non-schooled 1 (1.8)
Complete primary school 31 (55.3)
Incomplete primary school 7 (12.5)
Complete secondary school 15 (26.8)
Incomplete secondary school 1 (1.8)
No data 1 (1.8)
Father’s education
Non-schooled 1 (1.8)
Complete primary school 25 (44.6)
Incomplete primary school 6 (10.8)
Complete secondary school 9 (16.0)
No data 15 (26.8)

a Frequency was estimated in relation to the total number of homes with socio-environmental data (N=56).

Table 2 Hygiene practices of the child population from peri-urban neighborhoods of the city of Corrientes. 

Hygiene practices n (%)a
Frequency of bathing
More than once a week 20 (13.7)
Every day 126 (86.3)
Hand washing before eating and after using the restroom
Never 3 (2.0)
Occasionally 52 (35.7)
Always 87 (59.5)
No data 4 (2.8)
Nail maintenance
Short 119 (81.6)
Long 24 (16.4)
No data 3 (2.0)
Walk barefoot
Never 28 (19.1)
Occasionally 45 (30.9)
Always 68 (46.6)
No data 5 (3.4)
Play on the ground
Yes 75 (51.3)
No 67 (45.9)
No data 4 (2.8)

a Frequency was estimated in relation to the total number of children with data on hygiene practices (n=146).

Parasitological analysis

All fecal samples were examined at the Parasite Biology Laboratory of the Facultad de Ciencias Exactas y Naturales y Agrimensura of the Universidad Nacional del Nordeste (FaCENA-UNNE) in Corrientes, Argentina, using sedimentation and flotation concentration techniques 11. Graham’s method was used to evaluate the presence of Enterobius vermicularis eggs in children. The identification of the parasitic elements (eggs, larvae, cysts, oocysts) was based on their morphological characteristics and measurements. All families received the results of the parasitological diagnosis of the children in writing. A technical report with the results obtained from children and animals was also provided to the corresponding health authorities.

Statistical analysis

Univariate analysis

Frequencies and percentages were described by univariate analysis. Overall prevalence was calculated as the number of positive analysis units and parasitized hosts positive for at least one species divided by the total number of evaluated houses and analyzed hosts, expressed as percentages; specific richness was defined as the number of parasite species. We also calculated the percentage of monoparasitized and polyparasitized (two or more parasite species per host) participants.

Bivariate analysis

Fisher’s Exact Test was used to compare the two neighborhoods and evaluate the association between species pairs, as well as the relationship between age group, sex and parasitosis. Data analysis was performed in the R program (R Core Team 2022) 12.

The relationships between the age group of the children and the species found, as well as between sex and species were first evaluated by Multiple Correspondence Analysis. This allowed an overview of the relationships between the variables to then verify such associations (by means of a Chi-square test or Fisher’s exact test). The same method was used to analyze the relationship of socio-environmental characteristics with parasitosis and parasitic species and the relationship of hygiene practices with parasitosis and parasitic species. We did not perform multivariate analysis.

Ethical aspects

The study was approved by the Secretariat of Science and Technology of the Universidad Nacional del Nordeste (UNNE), Argentina. This research was conducted in accordance with Argentine laws. Sample collection was performed under official permissions in accordance with the Universal Declaration of Human Rights of 1948, the ethical standards established by the Nuremberg Code of 1947, the Declaration of Helsinki of 1964 and successive modifications, as well as the provisions of the National Law 25.326 on personal data protection.

FINDINGS

Dwellings

A total of 65 households with 164 children and 205 pets were recorded. At least 58 households (considered for analysis) provided a human and/or animal stool sample. We collected 146 samples from children and 101 from animals, representing a return rate of 89.0% and 49.2%, respectively.

At least one species of parasite and/or non-pathogenic organism from children and/or animal hosts was found in 54 dwellings (93.1%). The specific richness was 17 species, with a maximum of seven species in a single dwelling. The most prevalent protozoa were Blastocystis spp. and Giardia spp. in 60.3% and 43.1% of dwellings, respectively, while the most prevalent helminths were ancylostoma (46.5%) and Enterobius vermicularis (15.5%). A higher overall prevalence was found in neighborhood A (n=30) than in neighborhood B (n=28) (96.6% vs. 89.2%), but this difference was not statistically significant (p > 0.05).

Socio-environmental analysis

Socio-environmental data were obtained from 56 dwellings, in addition to data on personal hygiene practices of 146 children (Tables 1 and 2). We found statistical associations between solid waste disposal and the presence of Hymenolepis nana (p=0.024), as well as between the frequency with which participants bathed and the presence of Entamoeba coli (p=0.042) (Table 3).

Table 3 Variables selected by statistically significant association a 

Variables Parasitosis Parasitic species b
Hymenolepis nana Entamoeba coli
Age group
School-age children p=0.048 - -
Non-school-age children Reference - -
Solid waste disposal
Collected by the municipality - p=0.024 -
Open air or incineration - Reference -
Frequency of bathing
More than once a week - - Reference
Every day - - p=0.042

a Fisher’s exact test was used to evaluate the independence of the variables.

b The other parasitic species were evaluated, but only those with a significant association with the variables are shown.

Parasitological analysis in children

Seventy-two girls and 74 boys aged 0 to 14 years (45 not attending school and 101 attending school) were analyzed. At least one parasite species was found in 77 samples (52.7%). The specific richness was six species, with the protozoan Blastocystis spp. (35.6%) being the most prevalent species, followed by Giardia spp. (21.2%). We found a higher presence of parasites in children of school age (4 years and older) than in those who were not of school age (3 years and younger) (40.4% and 12.3% respectively; p< 0.05) (Table 4).

Most samples had a single parasite species, on the other hand, samples with multiple parasites had a maximum of four species. A statistically significant association was found between the presence of Giardia spp. and E. vermicularis (x2=7.3; p< 0.05).

Parasitological analysis in animals

A total of 101 fecal samples from domestic animals were analyzed; 68 (67.32%) had at least one parasite species. The specific richness was 15 species. Most of the animals analyzed presented only one parasite species (Table 4).

Table 4 General and parasite species prevalence in children (N=146) and animals (N=101) from two peri-urban neighborhoods of the Capital Department, Province of Corrientes. 

Groups or parasitic species Number of positive samples in children n (%) Age group Number of positive samples n (%) Number of positive samples in animals n (%)
School-age children Non-school-age children Dogs (n=84) Horses (n=8) Pigs (n=5) Cats (n=2) Rabbits (n=2)
Overall 77 (52.7) 18 (12.3) 59 (40.4) 60 (71.4) 2 (25.0) 4 (80.0) 1 (50.0) 1 (50.0)
Polyparasitized 28 (36.3) 6 (33.3) 23 (38.9) 16 (26.6) 0 1 (25.0) 1 (100) 0
Monoparasitized 49 (63.6) 12 (66.6) 36 (61.0) 44 (73.3) 2 (100) 3 (75.0) 0 1 (100)
Parasites
Protozoa 70 (47.9) 17 (11.6) 55 (37.6) 18 (21.4) 2 (25.0) 3 (60.0) 1 (50.0) 1 (50.0)
Blastocystis spp. 52 (35.6) 13 (8.9) 39 (26.7) 2 (3.5) 0 0 0 1 (50.0)
Coccidia 0 0 0 2 (2.3) 2 (25.0) 1 (20.0) 0 0
Eimeria spp. 0 0 0 1 (1.1) 0 0 0 0
Entamoeba coli 10 (6.8) 2 (1.3) 8 (5.4) 1 (1.1) 0 1 (20.0) 0 0
Giardia spp. 31 (21.2) 9 (6.1) 22 (15.0) 11 (13.0) 0 0 0 0
Iodamoeba bustschlii 0 0 0 0 0 1 (20.0) 0 0
Isospora canis 0 0 0 1 (1.1) 0 0 1 (50.0) 0
Helminths 24 (16.4) 4 (2.7) 18 (12.3) 53 (63.0) 0 2 (40.0) 1 (50.0) 0
Ascaris lumbricoides 3 (2.0) 1 (0.6) 2 (1.3) 0 0 0 0 0
Dipylidium caninum 0 0 0 2 (2.3) 0 0 0 0
Enterobius vermicularis 15 (10.2) 2 (1.3) 12 (8.2) 0 0 0 0 0
Ancylostoma 0 0 0 51 (60.7) 0 0 1 (50.0) 0
Hymenolepis nana 5 (3.4) 1 (1.3) 4 (2.7) 1 (1.1) 0 0 0 0
Oesophagostomum spp. 0 0 0 0 0 2 (40.0) 0 0
Spirometra spp. 0 0 0 2 (2.3) 0 0 0 0
Strongyloides larvae 0 0 0 1 (1.1) 0 0 0 0
Toxocara canis 0 0 0 7 (8.3) 0 0 1 (50.0) 0
Trichiuris vulpis 0 0 0 4 (4.7) 0 0 0 0

DISCUSSION

Infected animals eliminate parasitic stages through their feces and contaminate the environment 13. In this sense, our results show that 58.6% of the dwellings were contaminated with parasitic species (particularly geohelminths) found in animal feces, most of them with zoonotic potential. We found that 39.6% of the households were contaminated, in addition to the presence of parasitic species in children’s feces; 32.7% of the dwellings recorded only the presence of parasitic species in children’s feces (mainly zoonotic protozoa). Therefore, it is evident that in these dwellings the conditions for the development of the life cycle, maintenance and transmission of both helminths and protozoa were optimal and constitute a serious epidemiological scenario for public health.

Parasites were found in more than 50% of the children, most of them presented only one species. This coincides with previous research carried out in Corrientes 10,14 and other areas of Argentina 2,15. The most prevalent protozoan species were Blastocystis and Giardia (35.6% and 21.2%, respectively), while Entamoeba coli was the least prevalent (6.8%). This pattern has been reported in infant populations in Argentina 7 and in the province of Corrientes, with prevalence rates similar to our results 10; however, more recently, locally, the prevalence of Blastocystis has been found to be considerably lower (16.7%) 14.

Worldwide, Giardia is known to be one of the main parasites causing diarrheal diseases (not viral or bacterial) in humans and other mammals 16; while Blastocystis has been associated with different intestinal and extraintestinal diseases in humans 17. Entamoeba coli is commensal, but is an indicator of environmental fecal contamination. These three protozoa share the same fecal-oral transmission pathway and their presence is associated with contaminated water or consumption of raw vegetables with feces from infected hosts 18. Deficient personal hygiene habits, particularly hand washing, have also been described 19. In that sense, it has been reported that parents tend to over-report their children’s hand washing behaviors, which would systematically diminish any apparent benefit and in some cases may even show negative effects 20. In this sense, although mothers stated that most children washed their hands before eating and after leaving the bathroom, we found deficiencies in children’s general hygiene, a situation also reported by school authorities. Therefore, this type of result should be validated with a methodology that allows direct observation. Surprisingly, the presence of E. coli was associated with the frequency with which individuals bathed, but 86.3% of the mothers stated that their children bathed every day, supporting the need for direct observation.

As for animals, Giardia and Blastocystis were found in fecal samples from dogs (13.0% and 3.5%, respectively) and in one rabbit. Entamoeba coli was found in one dog and one pig. In the city of La Plata, Cociancic et al. 2) reported a similar prevalence rate in dogs for Giardia and a higher prevalence for E. coli (10.3%), but they did not find Blastocystis. The prevalence was even lower for these protozoa in dogs from another locality in Argentina 15. In short, despite the low prevalence of these parasites in pets, we establish the role of animals as a source of environmental contamination and disseminators or as possible foci of animal-animal or human-animal transmission, in which case molecular studies are necessary to verify possible cross-transmissions.

As for helminths, we mainly found Enterobius vermicularis (10.2%) and, to a lesser extent, Hymenolepis nana (3.4%) and Ascaris lumbricoides (2.0%). Enterobius vermicularis has been widely reported in all provinces of Argentina, with a prevalence rate ranging from 13.6% to 50.9% 14. Different studies associated its presence with onychophagia 2, poor nail and hand washing, overcrowding, and sharing beds and clothes 21. In our study, it is possible that the low prevalence is related to inefficient parental sampling.

Hymenolepis nana commonly infects humans and rodents. A prevalence rate similar to that found by our study has been reported in Argentina (14,22. In contrast, a prevalence rate higher than 20.0% was reported in the province of Misiones 7. Our results show that the presence of this parasite was associated with solid waste disposal. However, adults stated that garbage is collected in bags and then removed by the municipal collection service in all households where this helminth was found. It is important to note that we observed excessive accumulation of garbage both at the household level and in specific sectors of the neighborhoods evaluated. Therefore, there is evidence of inadequate waste disposal in this community, and we consider that this represents a risk, given the presence not only of rodents but also of domestic animals that were in direct contact with the waste.

A. lumbricoides was found in three children in three different dwellings. In contrast, a high prevalence of this parasite (38.9%) has been reported in other areas of Argentina 23. Its presence in the environment is mainly related to open defecation, climatic conditions and soil, the latter determining the viability and maturation of the eggs. In Brazil, Gonçalves et al. 24 determined the absence of latrines as a risk factor, showing that in South America, indigenous people usually live in conditions of extreme poverty.

Regarding the animals, ancylostoma, Toxocara canis and Trichuris vulpis were reported to be most prevalent in dogs (60.7%, 8.3% and 4.7%, respectively). This demonstrates high canine fecal contamination and poor pet health care in households. Similar results were reported in the city of Corrientes by Milano et al. 1, and higher values were reported in the city of La Plata by Cociancic et al. 3. Ancylostoma larvae and T. canis can be transmitted to humans and cause cutaneous larva migrans syndrome and neural larva migrans syndrome, respectively 25. Trichuris vulpis is a nematode of the large intestine of dogs and is of importance in veterinary medicine.

On the other hand, in agreement with Rivero et al. 15, co-infection of Giardia spp. and E. vermicularis was the most common and statistically significant, this could be due to the fecal-oral route of transmission that both parasite species share.

Regarding demographic variables, we found a significant association between age group and parasitosis, with school children being the group with the highest prevalence of parasites. Similar results have been reported by Rivero et al.15) and Navone et al.14 This finding could be attributed to the fact that schoolchildren maintain close contact with the foci of parasitic infection through play and insufficient hygiene habits 26.

The sample size was one of the limitations of our study, because we worked with a low number of dwellings and a low number of animal and human feces.

In conclusion, we found that a large number of the homes were contaminated with parasitic species, mostly helminths and protozoa of zoonotic importance, which shows the urgent need to improve sanitary control of children and animals in the area.

Acknowledgments

We thank all the people who offered their homes for sample collection and the school authorities, teachers and students who participated in this research. We thank Liliana Giménez for her professional assistance.

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Funding. This research was funded by the Universidad Nacional del Nordeste, through the project “Bio-ecology of protozoa and helminths of sanitary importance in synanthropic rodents, domestic animals and human populations of suburban areas of the city of Corrientes” (PI 20F007).

Cite as: Alegre RE, Gómez- Muñoz MdA, Flores-Lacsi EJ, Robles MdR, Milano F. Prevalence of intestinal parasites in children and domestic animals from two peri-urban neighborhoods in northeastern Argentina. Rev Peru Med Exp Salud Publica. 2023;40(4):466-73. doi: 10.17843/rpmesp.2023.404.12984.

Received: June 16, 2023; Accepted: October 18, 2023

Correspondence. Rumesilda Eliana Alegre; rumeeliana@gmail.com

Author contributions.

All authors declare that they meet the authorship criteria recommended by the ICMJE.

Conflicts of interest.

The authors declare that they have no conflicts of interest.

Roles according to CRediT.

REA: conceptualization, methodology, investigation, formal analysis, writing - original draft, writing - review & editing, project administration. MGM: conceptualization, methodology, investigation, writing - original draft, writing - review & editing. EJL: conceptualization, methodology, investigation, MRR: conceptualization, methodology, investigation. FM: conceptualization, methodology, investigation, writing - original draft, writing - review & editing, project administration, funding acquisition.

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