We studied patterns of intestinal parasite infections (i.e. schistosomes, soil-transmitted helminths and intestinal protozoa) in school-aged children in three settings of south Côte d’Ivoire; a rural, peri-urban and urban area. An important aspect of parasitic disease control programmes is the ability to readily identify and reach people at highest risk of infection and associated morbidity. Often, the poorest people are the least accessible ones living in remote rural areas, and hence they are at highest risk of parasitic infection and other conditions of ill-health [18–20].
In this study, the assessment of children’s prevalence and intensity of S. mansoni and soil-transmitted helminth infections was based on nine Kato-Katz thick smears derived from three stool samples. The day-to-day and intra-specimen variation in helminth egg output that compromise the sensitivity of the Kato-Katz technique, especially in areas of low infection intensity, is overcome by such a rigorous diagnostic approach [21–23]. However, multiple stool sampling to increase the sensitivity of the Kato-Katz technique for helminth diagnosis might result in reduced compliance. Indeed, particularly in the urban setting, compliance for providing all three stool samples was considerably lower than in the rural and peri-urban settings and this might have introduced some bias.
Another aspect of our study worth highlighting is the following. After our pre-screening based on a single stool sample, and then employing a more rigorous diagnostic approach, the previously anticipated S. mansoni endemicity levels were considerably overrun. As predicted by mathematical modelling  and confirmed in field studies, repeated stool sampling with multiple Kato-Katz thick smears prepared from individual stool samples, result in considerable increases of the observed prevalence of S. mansoni[21, 23, 25]. The same observations have also been made for soil-transmitted helminths [22, 26]. It follows that if rapid screenings are performed to reliably select a study setting or treatment scheme according to prevalence estimates, more sensitive diagnostic tools as alternatives to a rigorous sampling approach (i.e. collecting multiple stool samples and examining them with multiple Kato-Katz thick smears or other methods) are needed, particularly in areas with low transmission rates.
The current study confirms that schoolchildren from a rural setting are at higher risk of helminth infections than their counterparts living in peri-urban or urban settings. The remoteness of the rural setting, characterized by the absence of key infrastructures (e.g. tarmac road, health facilities, tap water and basic sanitation) play important roles. Our observations are in line with previous epidemiological surveys. Indeed, unsafe hygiene, water and sanitation and inadequate management of the environment exacerbate parasite infections in general, and helminth infections in particular [7, 19, 20, 27, 28]. Greatest differences between the prevalence of helminth infections, as a function of the study setting, were found with regard to the two schistosome species. Besides socioeconomic risk factors, the transmission of S. mansoni and S. haematobium is governed by intermediate host snails [6, 8, 29], and hence the availability of suitable snail habitats seem to vary considerably between the three settings even at this small-scale. While it is commonly believed that schistosomiasis is a “rural disease”, some studies have shown high prevalence in urban settings . Hence, detailed malacological investigations are needed to deepen our understanding of the epidemiology of schistosomiasis with regard to the level of urbanization. Interestingly, similar hookworm prevalences were found in the rural and peri-urban settings. This observation could be explained by the fact that the behaviour of the schoolchildren with regard to hygiene and faecal management in particular is similar. Since open defecation is widely practiced in these communities, efforts must be made to improve sanitation, which in turn will have major ramification on other neglected tropical diseases such as amoebiasis and giardiasis [28, 31].
Interestingly, the prevalence of intestinal protozoan infections among schoolchildren was found to be similar in the three settings. This might indicate that hygiene related to food consumption among schoolchildren is similar and needs to be improved. The two predominant intestinal protozoan species in the three settings under investigation are E. coli and E. nana. This observation is in agreement with previous studies done in different parts of Côte d’Ivoire [10, 31, 32].
Regarding intestinal parasite infection intensities, with the exception of S. mansoni in the rural setting, all other helminth infections were of light intensities whatever the setting. The observed moderate and heavy S. mansoni infections in the rural setting might be explained by high transmission in the absence of preventive and curative measures. Indeed, we are not aware of large-scale prior deworming activities in the district of Azaguié. There was a tendency of infection intensities of intestinal protozoa to decrease from rural to urban settings. Socioeconomic factors and educational attainment increase from rural to urban settings, and hence might explain the observed decrease in the intensities of intestinal protozoa.
Our study also confirms that multiparasitism is pervasive as observed elsewhere in sub-Saharan Africa and Asia [17, 33–37]. We found two children in the rural setting harbouring eight or 10 different intestinal parasite species concurrently. This high number of parasite species in a single host is an alarming situation, as multiple species infection may increase susceptibility to other parasites [38–40]. Associations between different parasite species, as well as the influence of age, sex and study setting, have been assessed in the current investigation. Of particular note is the strong positive association between S. mansoni and S. haematobium with an adjusted OR above four. Moreover, we found a significant association between S. haematobium and E. coli, which has not been described in the literature before. Boys and girls were at the same level of exposure to helminths and intestinal protozoa, except for hookworm, as boys showed significantly higher infection prevalence than girls. Interestingly, a previous study carried out by Keiser et al. (2002) in western Côte d’Ivoire found that hookworm infections were significantly more often diagnosed in girls [17, 35]. Behavioural and socioeconomic factors might explain this observed difference. Our study is in line with previous investigations that the risk of becoming infected with S. mansoni increases with age in children [41, 42]. To date, the effects of parasite interactions on the human body remain poorly understood. Without a deeper understanding of such parasite interactions, the effectiveness of parasitic disease control programmes are compromised.