Prevalence and risk factors of intestinal parasites among children under two years of age in a rural area of Rutsiro district, Rwanda – a cross-sectional study

Introduction This study aimed to assess the prevalence and associated risk factors of intestinal parasite infections among children less than two years of age in Rutsiro, Rwanda. Methods A cross-sectional parasitological survey was conducted in Rutsiro in June 2016. Fresh stool samples were collected from 353 children and examined using microscopy to detect parasite. A questionnaire was administered to collect data on hygiene, sanitation, socio-demographic and economic characteristics. Results Approximately one in two children (44.8%) were found to be infected with at least one intestinal parasite. Ascaris (28.5%) was the most prevalent infection followed by Entamoeba histolytica (25.95%) and Giardia lamblia (19.6%). Infection with more than one pathogen was noted e.g. presence of Ascaris and yeasts (8.9%), and amoeba with Trichocephale (4.4%), respectively. Children from non-farming families were less likely to be at risk of intestinal parasite infections (AOR = 0.41, p = 0.028) compared to children from farming families. Children from households with access to treated drinking water were less likely to contract intestinal parasite infections (AOR = 0.44, p = 0.021) compared with those who used untreated water. Children from families with improved sources of water were twice as likely to be diagnosed with intestinal parasitoses compared to those who did not. We postulate that the majority of families (50.1%) who have access to improved water sources do not treat water before consumption. Conclusion The high prevalence of intestinal parasitoses in children warrants strict control measures for improved sanitation, while treatment of drinking water should be considered.


Introduction
Intestinal parasite infections significantly affect public health in developing countries [1,2], and they are responsible for major morbidity and mortality throughout the world [3]. The reasons for the developing world being disproportionately affected includes over-crowding, poor environmental sanitation and hygienic practices [4]. Worldwide, approximately 3.5 billion people and 450 million people suffer from these infections, with children most affected and more likely to present with clinical symptoms [5,6]. Children may be infected with one or more of these intestinal parasites, affecting the child's immune system and increasing susceptibility to risk of other diseases. While mortality from intestinal parasite protozoan infections is relatively unusual, morbidity and indirect effects have significant consequences on health. These include gastrointestinal disorders, diarrhea, dysentery, vomiting, lack of appetite, hematuria, abdominal distension and mentally related health disorders, which can contribute to mortality [7].
Poor sanitation and inadequate hygiene [4,8]  Agriculture is the main source of income for the district.
Selection of study subjects: Samples of 353 children less than two years of age were randomly selected from all the households in the district. Firstly, we randomly selected 13 sectors in Rutsiro district, then from the selected sectors, we chose cells, which included designated villages termed "Imidugudu". Lastly, households were also selected using a systematic random sampling

Results
A total of 353 children under the age of two were selected for the study (Table 1). Microscopic stool sample examination revealed that approximately one in two children (n = 158, 44.8%) out of the 353 children surveyed were found to be infected with at least one intestinal parasite. The prevalence of Ascaris (28.5%) was the highest followed by amoeba (Entamoeba histolytica or coli) (25.95%), Giardia lamblia (19.6%), and yeasts (10.1%). Infection with more than one intestinal parasite such as Ascaris and yeast (8.86%) and amoeba with Trichocephale (4.43%) was noted, respectively. Other intestinal parasites detected such as Necator americanus and Trichomonas hominis were identified at less than one percent (0.63%) prevalence (Table 2). Of the 353 participants, half reported drinking untreated water (n = 177, 50.1%), 44% used drinking water from an unimproved source, and 31.4% stayed with livestock in the household ( Table 2). The factors associated with having any intestinal parasites included farming, water treatment, and water source (Table 3) (Table 4). Children from families with improved water sources were twice as likely to be diagnosed with intestinal parasite infections compared to those who did not have access to improved water sources. We postulate that this is because the majority of families (50.1%) who have access to improved water sources do not treat their water before use ( Table 2).

Discussion
Confirming the spread and level of intestinal parasite infections is very important in the design and implementation of appropriate prevention and control measures for child morbidity. This study was conducted to determine the prevalence of intestinal parasite infections and associated risk factors in children less than two years of age in Rutsiro district, a rural part of Rwanda. Almost half of the 353 children surveyed for intestinal parasite infections were found to be infected with at least one intestinal parasite. Ascaris was the most commonly identified with approximately one in three children infected with Ascaris. Furthermore, almost one in ten children were dually infected with Ascaris combined with other parasites and fungal organisms (amoeba and yeasts). In comparison to other intestinal parasites, the prevalence of Ascaris was comparable to the prevalence of Giardia duodenalis in a study assessing intestinal parasites among children [10]. This study of children in Rutsiro District indicates that apart from Ascaris, the prevalence of Giardia was higher than other intestinal parasites detected. Furthermore, the risk factors associated with intestinal parasite infection included farming occupation, drinking untreated water, and non-improved water sources. Children of farming parents were more likely to be infected with intestinal parasites compared to children of parents who did not farm. These parents were more likely to have an occupation which involved casual labour, food vending, or small commerce [11]. Although the prevalence of hookworm was high in the study subjects, data on the number of eggs per infected individual suggested that infection was at a low intensity.
Children from households with access to treated drinking water were less likely to have intestinal parasite infections, compared to those who drank untreated water. Surprisingly, we discovered that children from families with access to improved source of water were twice as likely to be diagnosed with an intestinal parasite infection compared to those from families without access to improved sources of water. It is possible that a significant proportion of mothers who receive water from trusted and improved sources of water do not treat the water before drinking it, a practice that would be mirrored by their children. As a result of the high prevalence of hookworm infection in the study subjects, an attempt was made to assess the association between hookworm infection and haematocrit values in the study subjects. In agreement with the previous report from southern Rwanda [11], the present study revealed there was no significant association between low haematocrit values and hookworm infection. In contrast, other studies have shown a strong association between low haematocrit values and hookworm infection [12,13]. This could be explained by low intensity of hookworm infection, nutritional status of the study subjects or due to differences in the species of hookworm [14].
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Conclusion
In conclusion, the study showed that intestinal parasites were prevalent in children less than two years of age in Rutsiro district, a rural and remote area of Rwanda. This calls for control measures such as community mobilization regarding water treatment, sanitation improvement, and maintaining regular adherence to deworming programs for children.

Competing interests
The authors declare no competing interests.

Acknowledgments
The authors would like to acknowledge the support of the Rwandan national laboratory, and the University of Rwanda through the Swedish program for financial support, which enabled data collection. The authors thank also the technical staff from the different health facility laboratories who supported the stool sample analysis.