Prevalence of Soil-Transmitted Helminths and Intestinal Protozoa among School Children in Lome, Togo

Background: Significant morbidity in children is associated with infectious diseases especially 
soil-transmitted helminth (STH) infections which are prevalent in sub-Saharan African countries. 
The objective of this study is to estimate the prevalence of STH and intestinal 
protozoa among schoolchildren in Lome, Togo. Patients and Methods: In 
November 2013, in each of the five districts of the Lome-commune region, thirty 
pupils per level of the third, fourth, fifth and sixth grades of five primary 
schools were included. Each child submitted a single stool sample that was 
analyzed by the Kato-Katz method for STH. In addition, stool samples of school children 
selected in third and sixth grades were examined by direct visualization using 
saline and Lugol’s stain for intestinal 
protozoa. Results: A total of 2944 children were enrolled at 25 
schools. The overall prevalence of STH at schools was 5.0% (range 1.5% to 
8.6%), was higher in boys than girls, and increased with age and grade. 
Hookworm was the most prevalent species (3.4% of children surveyed). Intestinal 
protozoa were found in 52.2% (765/1465) of children tested and commensal 
amoebae represented 22.7% of these protozoa identified. Entamoeba histolytica/dispar/moshkovskii and Giardia intestinalis were identified in 2.3% and 11.5% of children, respectively. Co-infestation was noted in 1.35% of children with intestinal helminths and 12.2% of children with 
protozoa. Conclusion: Although a high prevalence of intestinal protozoa 
was found in our study, the majority were non-pathogenic protozoa and the low 
prevalence of STH among school-age children 
in Lome-commune region confirms that mass drug administration (MDA) is 
not needed. Children should receive additional education on best hygiene 
practices.


Introduction
Soil-transmitted helminth (STH) infections and other parasitic diseases are prevalent in the world, particularly in sub-Saharan Africa. In 2017, the number of people infected in the world was estimated at 1.2 billion, with 90% of infections occurring in sub-Saharan Africa [1]. These parasites are often associated with stunted growth, micronutrient deficiency leading to decreased resistance to infection, cognitive impairment, educational difficulties among children and, later, low social and economic productivity [2]. Hookworm also causes anemia and increases maternal morbidity and low birth weight, thus maintaining a vicious cycle of morbidity and poverty [3]. School-age children (SAC) are the population most at risk, but they also contribute significantly to transmission. A key strategy recommended by WHO against these infections is morbidity control through mass drug administration (MDA) of preventive chemotherapy (PC) with albendazole or mebendazole targeting high-risk groups such as pre-school and school-age children, women of childbearing age and, since 2013, any adult at high risk [4]. PC should be conducted once per year if the prevalence in an ecological zone is between 20% and 49%, twice per year if it is 50% or higher, and individualized in communities with a prevalence of less than 20% [4]. In Togo, a national baseline survey conducted in 2009 found a high prevalence of STH [5] and in 2010, MDA with albendazole targeting SAC was initiated in areas where STH prevalence was 20% or more. During this baseline survey, the health region of Lomé-commune, considered at low risk regarding the urban setting, was not evaluated. However, urban areas with high STH prevalence have been noted in the literature [6] [7]. Since reliable current data were not available for this region with 1/7 of the entire population of Togo, field surveys to determine the disease prevalence within Lomé-commune were needed. This evaluation was carried out in order to assess the need for albendazole MDA in this region [8] [9] [10]. The objectives of this study were to determine the prevalence of Ancylostoma duodenale, Necator americanus, Ascaris lumbricoides and Trichiuris trichiura and the prevalence of intestinal protozoa among schoolchildren.

Characteristics of the Study Population
A total of 2944 students in 25 schools in the 5 districts in Lomé-commune region were enrolled. The mean age was 11 old years with a range from 7 to 16 years.
Characteristics of the surveyed population are shown in Table 1.

Prevalence of STH
Overall, 5.0% (148/2944) children tested positive for at least one STH. The prevalence of STH varied significatively across the five districts, from 1.5% in District N˚1 to 8.6% in District N˚2 (p < 0.0001) ( Figure 1).
Prevalence increased significantly with age; the highest prevalence was found in children over 15 years of age, 15.6% (p = 0.0001) ( Table 2). Infection was significantly more prevalent in boys than girls (5.7% vs. 4.4%; p = 0.049). Hookworm was the predominant STH infection with a prevalence of 3.4%. A. lumbricoides and T. trichiura were each found in 0.8% of cases.     Children in District N˚2 were significantly more likely to have intestinal protozoa than were the others (55.1% in district N˚2; p = 0.0412) (Figure 1).

Prevalence of Intestinal Protozoa
Among the intestinal protozoa found, the most common pathogenic protozoa were Entamoeba histolytica/dispar/moshkovskii, Giardia lamblia and Trichomonas intestinalis with an overall prevalence of 17.6% (Table 4).  this, finding a significantly higher prevalence of STH in rural and peri-urban areas than in urban areas [16]. Our results also showed that the highest district-level prevalence of STH in Lomé commune (8.6%) was indeed found in the district covering the peri-urban area of the capital. In contrast, Phiri et al. in Malawi in 2016 reported a significantly higher overall prevalence in urban than in rural areas (16.5% vs. 3.6%; p < 0.001) [17]. proved drinking water either on or off school grounds, having a handwashing station with water available, and access to a sex separate non-private or private latrine [18]. The variable distribution of these infections is therefore not always Open Journal of Pediatrics related to the urban or rural character of the survey area but may rather be related to the state of its environmental sanitation [15]. In addition, other factors could explain the disparity in results, especially the age of the subjects surveyed, their underlying state of health, socio-economic status and the parasitological tool and method used to identify the helminths.
The low STH prevalence in our study could also be due to the systematic deworming done in routine practice in the paediatric services of the health centers of Lomé.
The STH prevalence varied according to sex: 5.7% in boys versus 4.4% in girls (p = 0.049). This male predominance has been reported in several studies [19] [20], while others have noted a female predominance [8].
STH prevalence in our study also increased significantly with age (p = 0.0001) and consequently with grade level. This result is likely due, in part, to the residual impact on the younger age groups of the albendazole deworming campaigns organized annually by the national nutrition program, with the support of UNICEF, for children under 5 years of age [21].  [8]. However, these results contrast with those of N'diaye et al. [20] in Senegal where A. lumbricoides and T. trichiura were the predominant species with a prevalence of 60% and 25.6% respectively. Local ecology and the history of distribution of ivermectin in countries co-endemic for onchocerciasis may play a role in this disparity.
The low prevalence and intensity of infestation observed in our study support the decision not to extend mass treatment with albendazole to this region of Lomé-commune.

Prevalence of Protozoa
The nested survey of intestinal protozoa in 3 rd and 6 th grade children was included to provide information on the prevalence of these infections, which have not previously been examined in this region; 52.2% of pupils surveyed were positive for at least one protozoan in our study. Our prevalence is higher than the 34.7% prevalence found among children under 5 years of age in South Africa [25] and 25.2% in Rwanda [26]. This difference is likely due to the fact that in our study all identified parasites (pathogenic and commensal protozoa) were accounted for, while the other authors focused their evaluations only on pathogen species. However, the prevalence of protozoa in Togo is lower than that reported in some Maghreb countries: 96.5% in Sfax in Tunisia [27] and 88.3% in Kenitra in Morocco [28]. This difference could be related to the diagnostic techniques (parasite concentration and/or molecular or immunological tools) used Prevalence of intestinal protozoa varied by district; the highest rates were observed in peri-urban areas (districts 2 and 3) where access to latrines is poorer and where individual and collective hygiene practices are less frequently observed.
The pathogenic species Entamoeba histolytica/dispar/mishkovskii, Giardia intestinalis and Trichomonas intestinalis were found at relatively low rates, 2.3%, 11.5% and 3.8% respectively. Our results are similar to those of Chekhrouhou [27] who reported these species in 2.2%, 17% and 1.5% respectively, and those of Ghenghesh in Libya, for the period 2000-2015, who noted 6% of E. histolytica/dispar/moshkovskii, 2% of G. lamblia and 0.9% of Cryptosporidium spp. [29]. Much higher prevalence of E. histolytica/dispar/moshkovskii has been described worldwide [29] [30]; the most commonly identified commensal species were E. nana and Entamoeba coli, with prevalence of 65.5% and 62.3%, respectively [30], similar to our study where E. coli was the most prevalent commensal amoebae (16.5%). In South Africa, Samie et al. were able to differentiate between the three species of the E. histolytica complex in 170 samples using the Polymerase Chain Reaction (PCR) technique and noted 15.9% E. moshkovskii, 14.7% E. dispar and 4.1% E. histolytica [31]. This finding suggests that the proportion of pathogenic species in our study might have been much lower had we used PCR to differentiate the non-pathogenic and pathogenic species of E. histolytica complex.
The prevalence of pathogenic intestinal protozoa in our study does not constitute a public health problem in the Lomé commune health region, similar to our findings for STH.

Conclusion
The low prevalence of STH among pupils in the Lomé-commune health region shows that, despite variability between districts and schools, with urban areas having relatively lower prevalence than more rural areas, the WHO threshold for implementing albendazole mass drug administration is not reached. Low prevalence of pathogenic intestinal protozoa was also found. Intestinal parasites and especially STH, therefore, do not appear to constitute a significant public health problem in the Lomé-commune region. Nonetheless, SAC in this region should be treated three times during their primary school period in accordance with the WHO guidelines and emphasis placed on hygiene education and awareness-raising for the elimination of these intestinal parasites in Togo. Open Journal of Pediatrics

Limitations
This work is submitted for publication after several years as a 5-year evaluative study was planned in 2018. Due to lack of funding it has not yet taken place. It was therefore imperative for us to report on the first stage of the project conducted in 2013. The data presented in this manuscript may no longer represent the current situation of the prevalence of these potentially evolving STH, but the study had the merit of showing that this health region where the Togolese capital is located does not need MDA of albendazole to SAC.