Intestinal parasitosis caused by protozoa and helminths (e.g. Giardia lamblia, Blastocystis sp., Ascaris lumbricoides, hookworms – Ancylostoma duodenale and Necator americanus) are the most common infections among neglected infectious diseases23. It is estimated that more than 3500 million people, mainly children from developing countries, are infected with intestinal parasites. Parasitic infections can cause diarrhea and intestinal malabsorption, and in the most severe cases may affect the physical growth and intellectual development of children, as well as the labor productivity of adults12,30.

The transmission of intestinal parasites is generally considered to be “mediated by the environment”, which suggests that they are particularly sensitive to the changes that occur in it11. In this context, several studies showed an association between intestinal parasitosis and environmental factors (e.g. temperature, precipitation, vegetation indices)4–6,16,27. In particular, it is not surprising to observe that the prevalence of parasitic infection varies among locations due to the environmental diversity present in Argentina, with an evidently decreasing trend from north to south and from east to west3,8,9,18–20,28.

Despite the available information that explains the differences in the prevalence of enteroparasitosis, there are limited studies on the relationship with environmental variables4. For this reason, the present study aimed to evaluate the environmental variables that represent risk factors for parasitic infection in children and youth populations in Argentina.

The Pearson's test was performed to assess the correlation between the environmental variables, using a correlation coefficient >0.75. Data source, spatial resolution and maximum correlation values of the selected variables are summarized in Table 1. Subsequently, the linearity of each environmental variable with respect to the parasitic logit was analyzed using dispersion diagrams. The variables that showed a linear relationship were evaluated by generalized linear models, considering those that presented a lower Akaike information criterion as better models. The variables that showed a non-linear relationship were analyzed using generalized additive models and it was considered a good model if it presented an explained return greater than 70%. Odds ratio (OR) values and their respective 95% confidence intervals (95% CI) were calculated. The goodness of fit of the final model was evaluated using the Hosmer–Lemeshow test and a p value >0.05 indicated an adequate model. All statistical analyses were performed using the R software.

The study was performed without affecting the physical, psychological and moral integrity of the participants and protecting their identity. This research was approved by the Comité de Ética de la Escuela Latinoamericana de Bioética (CELABE) under Resolution No. 003/2016, Record No. 73. The study was conducted in accordance with 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. Special attention was also paid to Article 5 of the Regulation Decree of National Law 25.326.

Of the total population analyzed, 66.9% (2633/3937) were parasitized by at least one parasite species. Protozoan infection was more frequent than helminth infection (52.7% and 39.6%, respectively). The total number of identified parasite species was 17 and the most prevalent ones were Blastocystis sp. (42.2%), Enterobius vermicularis (33.6%) and Giardia lamblia (17.0%). Moreover, 7.7% were parasitized with at least one geohelminth species, hookworms and Strongyloides stercoralis (4.3% and 3.0%, respectively) being the most frequent. Entamoeba coli was the most prevalent non-pathogenic species (12.9%) (Table 2).

The highest prevalence of intestinal parasitosis was observed in Misiones (82.1%) and Formosa (78.1%), followed by Buenos Aires (66.8%), Mendoza (61.8%), Entre Ríos (58.6%) and Chubut (38.7%). Protozoan infection was more prevalent in Formosa (71.9%) and Misiones (68.0%), and less prevalent in Chubut (24.7%). Blastocystis sp. was more frequent in Misiones (59.6%) and Formosa (57.9%) and less frequent in Chubut (17.5%). The highest prevalence of infection by G. lamblia was observed in Formosa (37.7%) and Misiones (20.2%), and the lowest prevalence was found in Chubut (6.1%). Geohelminth infection was more prevalent in Misiones (23.3%) and Formosa (17.5%), and was absent in Chubut. Among the geohelminth species, Ascaris lumbricoides and Trichuris trichiura were more prevalent in Formosa (7.9% and 7.0%, respectively), and hookworms and S. stercoralis in Misiones (16.2% and 11.1%, respectively) (Table 2).

Infection by protozoa, and by G. lamblia in particular, was greater when the mean summer temperature was higher (OR=1.2 for both). On the other hand, it was observed that for each increase in isothermality, the risk of infection by Blastocystis sp. increased (OR=1.1). Isothermality was also associated with an increased risk of geohelminth infection (OR=1.2). The risk of infection with A. lumbricoides was associated with an increase in the mean temperature of the wettest quarter (OR=1.2). On the other hand, infection by hookworms was associated with an increase in NDVI (OR=32.5) (Table 3). Fig. 2 shows the parasitic logit with respect to each environmental variable. In Misiones province, 45.5% of the participants infected by hookworms lived in areas with abundant arboreal-shrubby vegetation, and 36.4% in areas with vegetation of agropastoral use. In contrast, a minor proportion of infected participants lived in urban areas (18.2%). However, in Formosa province, 66.7% of the infected participants lived in urban areas and 33.3% in areas of vegetation of agropastoral use (Fig. 1a and b).

Figure 2.

Risk variables in relation to logit of infection with protozoa (a), Blastocystis sp. (b), Giardia lamblia (c), geohelminths (d), Ascaris lumbricoides (e) and hookworms (f).

(0.21MB).

The present study shows that the intestinal parasitosis found in the populations analyzed are associated with environmental factors related to the temperature and soil characteristics in the different study areas.

The risk of infection by protozoa and, by Giardia lamblia in particular, was associated with the mean temperature in the summer months. Other studies showed an increased risk of giardiasis when the temperature increased1,16. Warm temperatures can prolong the infective period of cysts and facilitate transmission through reservoirs and vectors or through intensified pathogen-host interactions. Likewise, the expected global increase in temperature and rainfall could favor the survival and dispersion of cysts, exposing new populations to parasitic infection. Likewise, an increase in temperature could also favor infection by other pathogens (e.g. Cryptosporidium spp.), which have the same mode of transmission and that have been positively associated with higher temperatures16.

The risk of infection by Blastocystis sp. and geohelminths was positively associated with isothermality. It is known that extreme temperature conditions could adversely affect the survival of parasitic forms present in the environment. On one hand, the cystic form of Blastocystis sp. can survive for one month at room temperature and two months at 4°C. Although this is the most resistant form of Blastocystis sp., this parasite is affected by extreme temperatures. In contrast, the vacuolar form frequently found in feces is highly sensitive to changes in temperature14,29. On the other hand, embryonic development of geohelminths occurs within defined temperature limits between 28 and 32°C, suggesting that extreme values could inhibit the development and therefore the infectivity of these species2.

It has been observed that as the mean temperature in the wettest quarter increased, the risk of infection with Ascaris lumbricoides was greater. Similarly, Chammartin and collaborators observed that the risk of infection was higher due to an increase in the mean temperature in the warmest quarter6. Similar results were found in Malaysia, where the mean soil surface temperature was positively associated with the infection; however, the minimum and maximum temperatures showed a negative association21. Likewise, Brooker and collaborators reported that in Uganda the highest prevalence was observed in areas with temperatures of 30°C and it decreased in areas where the temperature exceeded 38°C2. This result was attributed to the effects of extreme heat and insufficient humidity on egg survival and embryonic development.

The risk of infection with hookworms became higher as the NDVI increased. Similar results were found in Brazil and South Africa26,27. In contrast, a negative association was observed between the NDVI and hookworm infection; however, in China, a positive association with A. lumbricoides and Trichuris trichiura infection was reported15. However, other studies stated that geohelminthiasis is generally frequent in areas with forest cover because forests provide shade and prevent desiccation of the soil surface, thus protecting the larvae from solar radiation21,25.

In Argentina, a bibliographic review conducted by Juárez and Rajal (2013) reported that there is a coincidence between the parasite species found in both fecal and environmental samples12. This finding suggests that parasites that can cause intestinal disorders in humans can be isolated from samples of water and soil that are exposed to different environmental conditions. The intestinal parasites found in this study are indicative of the different climatic-environmental conditions present in Argentina. The present study generated knowledge about the environmental factors that are associated with an increased risk of parasitic infection. Thus, it strengthens the development of control and prevention strategies that would improve the quality of life of the most vulnerable populations.

This work was funded by the Universidad Nacional de La Plata (UNLP-11/N 679 y N759), Agencia Nacional de Promoción Científica y Tecnológica (PICT 1541) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 734, PIO N13420130100004CO).

The authors declare that they have no conflicts of interest.