Introduction

Intestinal parasitosis is considered a public health problem that affects individuals of all ages and sexes; however, it occurs mainly in the first years of life, since this age group has not yet acquired the necessary hygienic habits to prevent it and has not developed immunity against the different types of parasites¹.

Numerous investigations have pointed out the association between poverty and health limitations, which is reflected in high parasite prevalence rates. In humans, intestinal parasitosis causes, among other gastrointestinal alterations, eosinophilic colitis, diarrhea, dysentery, decreased growth rate due to malabsorption syndrome, anemia, and modification of the intestinal microbiota, which in most cases leads to low intellectual performance and decreased work capacity in the affected individuals². Clinical manifestations can vary from asymptomatic to severe cases, which rarely lead to death³.

Parasitic infections are widespread, and their prevalence today is similar to that which existed 50 years or more ago in many regions of the world. This is because of the complexity of the epidemiological factors that condition them and the difficulty in controlling or eliminating these factors⁴.

The prevalence in Ecuador is similar to that in other Latin American countries with similar climatic characteristics, unhealthy conditions, and poverty. In the country, unspecified intestinal parasitosis was among the main causes of outpatient morbidity in the Ministry of Public Health of Ecuador in 2016, and among the top ten causes of pediatric consultation⁵, epidemiological differences existed depending on the area of the country studied.

Escobar et al.⁶ studied 610 children under 12 years of age from San Luis-Chimborazo, in which 91.48% showed the presence of parasites, detecting 30.36% of Entamoeba coli, Entamoeba histolytica 19.02%, lodamoeba bütschlii 2.79%, Chilomastix mesnili 3.93%, and Giardia lamblia 5.08%. Ramos and Fiallo⁷ analyzed 50 individuals in the Flores parish of Riobamba canton, finding 100% of parasitized individuals, and detected Entamoeba histolytica as the main species. González et al.⁸ performed a parasitological analysis of 296 individuals, residents in six communities of the San Andrés parish in Riobamba, and revealed that 98.2% of them were infected.

At the regional level, the number of cases is lower than those reported for other provinces. Durán et al. report for the Pajan canton (Manabí)⁹, a 45.30% prevalence of intestinal parasites, with a predominance of the Entamoeba complex species with 26.50%, in the child population studied. Murillo et al.¹⁰ demonstrated a 30.59% prevalence, with a predominance of monoparasitism, agreeing with the Entamoeba complex species as the most prevalent, when studying children from Jipijapa. Véliz et al.¹¹ studied 168 schoolchildren from Puerto Cayo, Machalilla, and Puerto López, and reported that the highest prevalence was detected in Machalilla (1.76%), Puerto López (0.67%), and Puerto Cayo (0.31%).

In the country, there is a varied prevalence of enteroparasites in the child population; however, children and adolescents from the rural area of Rocafuerte had not been previously evaluated by parasitological diagnosis; therefore, the present study was carried out in individuals from three rural communities of Rocafuerte, Ecuador.

Materials and methods

Study area:

The Rocafuerte canton is located in the western part of the Ecuadorian territory, central part of the Province of Manabí, at 0° 55" and 6" south latitude and 80° 26" 10" western longitude, bordering to the north with the cantons Sucre and Tosagua, to the south with Portoviejo, to the east with Junín and to the west with Portoviejo and Sucre. Its topography is flat, its maximum height is 215 m above sea level, the climate is relatively cool, and it has an average annual temperature of 25 °C. With an average rainfall of 163.5 mm and a relative humidity of 84%, it is classified as Tropical Thorny Mountain and Tropical Very Dry Forest. It covers 54 communities divided into three areas: upper, lower, and urban. Its main economic activities are related to the sale of creole sweets as well as agriculture, mainly planting corn and rice¹². See Fig. 1

Figure 1 Location of Manabí in Ecuador and Rocafuerte within Manabí Fountain: Wikipedia 

Results

Of the 154 individuals studied (n = 154), 79 (51%) were male and 75 (49%) were female, with an average age of 10.3±SD 3.2 years. A predominance of non-parasitized individuals was observed in 54.50% (84/154) of the parasitized individuals and 70/154 (45.50%) in the sectors studied. Although there was no significant difference (p>0.05), a greater number of parasitized individuals were determined in the male sex and age group of 6 to 11 years. Regarding the sector studied, a greater number of parasitized individuals was detected in El Frutillo, followed by Higuerón, and to a lesser extent El Cerrito, with a significant difference in relation to this variable and the presence of parasitized individuals (p=0.004) (Table 1).

Regarding parasitic associations, the number of children with a single parasitic species was 47, representing a percentage of 67.14%, while there polyparasitized were 23 individuals (32.86%). In most cases, an association of two species of parasites was found (82.60%), with the association of four species (4.35%) being infrequent. All parasitic associations (2, 3, and/or 4 species) were observed in males, whereas in females, only two species were associated. When polyparasitism was compared by sex, a significant difference was observed (p=0.015).

Table 2 shows the parasitic species found, where the predominance of protozoan/chromist species over helminths is notable. Likewise, it is observed that the species Blastocystis sp. with 24.03%, followed by the commensals Endolimax nana and Entamoeba coli (13.64%/9.74%, respectively). Fourteen individuals with Giardia lamblia cysts (9.09%) and 6 with the Entamoeba complex (3.90%) were detected. Regarding intestinal helminths, Enterobius vermicularis was detected in only four individuals (2.6 %). Furthermore, at the community level, significant differences were found in the prevalence of E. vermicularis in Higuerón (p=0.006) and E. coli in El Cerrito (p=0.029).

Discussion

The prevalence of intestinal parasites (45.5%) is similar to that reported in other studies carried out in the country, where similar figures have been reported in the child population^17-20. Likewise, the predominance of monoparasitized individuals was observed; a similar situation demonstrated by Cuenca et al.²⁰ in the child population in Paute, Ecuador, detecting a percentage of monoparasitized individuals of 63.64%. Other investigations carried out on the same population in other areas of the country also reported a greater number of individuals with a single parasitic species^9-11. A low percentage of polyparasitized individuals was detected; however, the difference between mono-and polyparasitized individuals was significant according to sex.

The observed difference could be attributed to some activities carried out by male individuals, who are more exposed to an environment contaminated with parasitic forms. When investigating this, it was found that the majority of male children and adolescents attend sports schools promoted by the cantonal government, who could have greater contact with contaminated environments when carrying out sports activities, being a risk factor for acquiring intestinal parasites. However, risk factors should be evaluated in detail to provide definitive conclusions.

The most prevalent species was Blastocystis sp., a microorganism belonging to the kingdom Chromist²¹, while the most frequent protozoan was Endolimax nana. Other microorganisms detected in the fecal samples were E. coli, G. lamblia, Entamoeba complex, and Chilomastix mesnili, indicating that the main parasites carried by the individuals were protozoa/ chromists. Of the helminths, Enterobius vermicularis was the only one diagnosed in four cases. It is important to note that 2 of the reported cases of E. vermicularis were identified through macroscopic fecal examination; since female adults were observed moving on the surface of the feces, this finding was fortuitous. This highlights the importance of performing a detailed macroscopic examination of the stool.

The high prevalence of protozoan/chromist species compared to helminth species is notable; this is important, since fecal concentration procedures were used, which increases the possibility of the recovery of evolutionary forms of helminths²². This is relevant since many of the publications carried out in the country only include fecal microscopic examination, which has a low sensitivity compared to concentration methods^22-24. When compared with previous studies of intestinal parasitosis in children from Ecuador, it is observed that the predominance of protozoa in fecal samples is common^9-11,17,25. Thus, this study supports the idea that pro-tozoan/chromist parasitosis is a public health problem at regional and national levels, more so than helminth infections. An explanation for this could be the transmission of protozoa/chromists through drinking water as a risk factor. Water resources are one of the problems faced by the population of the Rocafuerte canton, both in quantity and quality. The lower area, being crossed by the Portoviejo and Chico Rivers, has water throughout the year, but due to the pollution of the rivers, the water is of poor quality. In the upper area, on the other hand, they only have water in winter and if the winter is good, they can store water for the rest of the year. According to INEC 2022¹³, 80.4% of Rocafuerte receives water from the public network, and the remainder receives water through other means of supply, such as wells, rivers, springs, delivery cars, and rain.

González et al.²⁶ parasitologically evaluated irrigated, piped, and stagnant water from an agricultural area of the Ecuadorian Andes, finding in the three types of water, protozoans (70.56%), followed by chromists (40.65%) and helminths (13.08%). Among the transmissible parasites, the following stand out: Blastocystis spp. (40.65%), free-living amoeba (5.61%), and Entamoeba spp. (8.41%), Giardia duodenalis (6.54%), Balantidium spp. (13.51%), Cryptosporidium spp. (17.76%), Cyclospora spp. (3.74%), Cystoisospora spp. (2.34%), Eimeria spp. (13.55%), Dibothriocephalus spp. (0.47%), and nematode larvae (13.08%). This study demonstrates the probability of ingesting contaminated or untreated water in some communities in Ecuador.

It is important to note that Blastocystis sp. has been identified as the main microorganism detected in the feces of children, a place that was previously occupied by Giardia intestinalis, which was always identified as the most frequent protozoan in this age group^27-29. De la Torre et al.³⁰, when evaluating the fecal matter of 153 children from the Ambato canton, Ecuador, point out an important predominance of protozoa/chromists, with the most frequent causal agent being Blastocystis sp. (47.60%), followed by Entamoeba coli (32.03%) and Endolimax nana (28.01%). In their study, Llerena et al.³¹ evaluated schoolchildren from semi-rural areas in Ecuador, pointing out Blastocystis sp. (10%) as the most common species, followed by Endolimax nana (3.7%) and Entamoeba complex (2.5%), which is similar to the present study. A recent publication on schoolchildren from Chimborazo and Guayas determined that the main parasites detected were Blastocystis 39.2% and E. vermicularis (16.7 %)³².

It is worth highlighting the significant difference found between the prevalence of enteroparasites per community studied, with Frutillo being the one that presented the highest percentage. The parents of the children in this sector stated that they had not been to the doctor lately and had not given them antiparasitic treatment in the last 6 months, while in the other communities (El Cerrito and Higuerón), they reported having dewormed the children and adolescents months ago, the reason for which these findings could be attributed. However, it is necessary to investigate the risk factors that may influence the increase in cases in this sector.

Statistical differences were observed between the parasitic species and communities. Enterobius vermicularis was detected only in Higuerón, which suggests overcrowding conditions in this sector, as this is one of the risk factors for this parasitosis^32-36. However, it should be clarified that, to have a real conclusion of this situation, appropriate laboratory procedures for this parasite (plastic tape method/Graham test) and a community survey must be carried out. Although a significant difference was also detected in relation to E. coli, owing to the absence of cases in the El Cerrito community, in general terms, this community presented the lowest number of cases of intestinal parasitism.

Knowing the species of intestinal parasites carried by children and adolescents in Rocafuerte is essential to guarantee their health and well-being. Early detection of these infections allows for timely treatment and prevents complications such as malnutrition, developmental delay, anemia, learning problems, and other conditions that negatively impact an individual's quality of life. Education about hygiene habits and access to diagnostic and control methods is essential to combat these infections and ensure optimal physical and cognitive development in children and adolescents.

It should be noted that this research was a descriptive study; therefore, the potential determining factors that allowed infection with parasites were not analyzed, nor were the clinical manifestations of the participants, which can be considered a limitation of the project.

In conclusion, the medium prevalence of parasitosis found in this study reflects the predisposition of these communities to intestinal parasites produced by protozoa/chromists, possibly related to the ingestion of contaminated/untreated water in the population studied.