https://orcid.org/0000-0002-0129-7323
Figures
Abstract
Background
Schistosomiasis and hookworm infection remain public health problems in large parts of sub-Saharan Africa. The epidemiology of schistosomiasis and hookworm was studied in seasonal transmission settings in the northern part of Côte d’Ivoire.
Methodology
In August 2018, a cross-sectional study was conducted. Urine and stool samples were collected from 742 individuals aged 6–96 years in 16 localities from four departments in northern Côte d’Ivoire. Urine samples were examined by a filtration method for quantification of Schistosoma haematobium eggs. Stool samples were subjected to duplicate Kato-Katz thick smears and eggs of Schistosoma mansoni and soil-transmitted helminths (STHs) were counted. Additionally, a questionnaire was administered to determine demographic characteristics and to identify risk factors of schistosomiasis and STHs. Malacologic surveys were carried out at water points that are contacted by humans and animals.
Principal findings
The prevalence of schistosomiasis was very low. Only two cases of S. mansoni were found (0.3%, 95% confidence interval [CI]: 0.1–1.0%). The distribution of S. haematobium was focal, with cases found only in two departments; Ferkessédougou (5.4%, 95% CI: 2.5–9.9%) and Ouangolodougou (2.7%, 95% CI: 0.9–6.3%). Hookworm was the only STH species observed with a prevalence of 1.5% (95% CI: 0.8–2.8%). A higher risk of S. haematobium infection was observed in males compared to females, but the difference was not statistically significant (2.3% versus 1.3%, odds ratio [OR]: 1.5, 95% CI: 0.8–2.7). Participants aged 16–20 years showed the highest prevalence of S. haematobium. A total of 111 human- and animal-water contact points were identified at 47 water sources. Three potential intermediate host snails of schistosomes were collected; namely, Bulinus forskalii (n = 761), Bulinus truncatus (n = 205), and Biomphalaria pfeifferi (n = 1). Yet, only one specimen of Bu. truncatus was found to be shedding schistosome cercariae.
Conclusions/Significance
This study confirms very low transmission of schistosomiasis and hookworm in northern Côte d’Ivoire. The establishment and rigorous implementation of integrated surveillance-response systems could lead to the elimination of schistosomiasis and hookworm in this part of Côte d’Ivoire.
Author summary
Schistosomiasis and soil-transmitted helminthiasis, the latter including, hookworms, roundworms, and whipworms, are the most widespread parasitic neglected tropical diseases. As is the case in many sub-Saharan African countries, schistosomiasis and soil-transmitted helminthiasis are endemic in Côte d’Ivoire. Mass drug administration is the mainstay of the global control strategy against schistosomiasis and soil-transmitted helminthiasis and has been implemented in Côte d’Ivoire since 2013. The new road map put forward by the World Health Organization (WHO) for the control of neglected tropical diseases aims to eliminate schistosomiasis and soil-transmitted helminthiasis as a public health problem by 2030. In light of WHO’s goals, this study updates prevalence data for schistosomiasis and soil-transmitted helminthiasis and provides a deeper understanding of risk factors that drive transmission in the northern part of Côte d’Ivoire. The findings showed very low prevalence and transmission of schistosomiasis and hookworm. Participants aged 16–20 years and fishermen had the highest prevalence of urogenital schistosomiasis, with both males (2.3%) and females (1.3%) at risk of infection. The results corroborate findings from other investigations in sub-Saharan Africa, which confirm that current efforts to control schistosomiasis and soil-transmitted helminthiasis are successful. Nevertheless, further investment is still needed to reach elimination. In particular, a surveillance-response system would be a valuable tool in a low-prevalence context such as northern Côte d’Ivoire.
Citation: Kouadio JN, Giovanoli Evack J, Sékré J-BK, Achi LY, Ouattara M, Hattendorf J, et al. (2023) Prevalence and risk factors of schistosomiasis and hookworm infection in seasonal transmission settings in northern Côte d’Ivoire: A cross-sectional study. PLoS Negl Trop Dis 17(7): e0011487. https://doi.org/10.1371/journal.pntd.0011487
Editor: Jong-Yil Chai, Seoul National University College of Medicine, REPUBLIC OF KOREA
Received: March 17, 2023; Accepted: June 29, 2023; Published: July 17, 2023
Copyright: © 2023 Kouadio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript.
Funding: JU was supported by the Swiss National Science Foundation (SNSF, https://www.snf.ch/en) through a grant. The grant number is: 31003A_170113. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Schistosomiasis is a chronic parasitic disease caused by infection with trematode worms of the genus Schistosoma [1]. Schistosomiasis has a complex life cycle, involving freshwater snails as intermediate host, and human and other mammals as definitive hosts. Schistosomiasis remains a public health problem in tropical and subtropical regions of Africa, Asia, the Caribbean, and South America [2]. An estimated 779 million people are at risk of acquiring schistosomiasis [2], with some 241 million people requiring preventive chemotherapy in 2020 [3]. In 2018, the estimated global burden of schistosomiasis was 1.4 million disability-adjusted life years (DALYs) [4]. More than 90% of schistosomiasis cases are concentrated in sub-Saharan Africa, where the most relevant human-pathogenic species are Schistosoma mansoni and S. haematobium. As is the case with many neglected tropical diseases (NTDs), schistosomiasis primarily plagues marginalized communities, where there is no or only limited access to clean water and improved sanitation [5]. Following a World Health Assembly (WHA) resolution put forward in 2001, considerable resources have been dedicated to prevent and control schistosomiasis in humans, mainly by means of morbidity control through preventive chemotherapy with praziquantel. Over the past 15 years, schistosomiasis has decreased significantly in many countries in sub-Saharan Africa [6]. In order to contribute to the attainment of Sustainable Development Goal (SDG) 3, that is to ensure healthy lives and promote well-being for all at all ages, the new WHO road map targets the elimination of schistosomiasis and soil-transmitted helminthiasis (STH) as a public health problem by 2030, and the interruption of schistosome transmission in humans in selected countries by 2030 [7]. STH is caused by parasitic worm infections with three main species, namely Ascaris lumbricoides, hookworm, and Trichuris trichiura [8,9]. In 2018, the global burden of STH was estimated at 1.9 million DALYs [4]. Schistosomiasis also affects the livestock sector and hybrids between livestock and human schistosome species have been reported in humans [10–12].
In Côte d’Ivoire, schistosomiasis is endemic and caused by infection with S. mansoni and S. haematobium [13,14], with Biomphalaria and Bulinus serving as intermediate host snails, respectively. In 2013, the national prevalence of S. mansoni in school-age children was 37.7% based on an analysis of historical data [15]. Over the past decade, a preventive chemotherapy program was implemented, mainly targeting school-age children [16]. Consequently, the prevalence of schistosomiasis has declined, also in the northern part of the country, where transmission is seasonal [17]. Of note, livestock schistosomiasis is endemic in Côte d’Ivoire with high prevalences observed in the North [18]. In light of the new WHO road map, it is important to update the distribution of schistosomiasis and STH and deepen the understanding of risk factors that drive transmission.
This study aimed to assess the epidemiologic characteristics of schistosomiasis and STH in northern Côte d’Ivoire. The specific objectives were to determine the prevalence, distribution, and risk factors of schistosomiasis and STH. Particular emphasis was placed on freshwater snails in human- and animal-water contact sites. The study was part of a larger One Health project investigating transmission dynamics of schistosomiasis and fascioliasis across host species in Côte d’Ivoire [18–20]. The results will inform the national control program to refine strategies with the ultimate goal of interrupting the transmission of schistosomiasis and STH in northern Côte d’Ivoire.
Methods
Ethics statement
Ethical approval was obtained from the National Ethics and Research Committee of Côte d’Ivoire (reference no. 035/MSH/CNER-kp) and the Ethics Committee of North-Western and Central Switzerland (reference no. UBE-2016-00707). District and local authorities, village chiefs, community members, and eligible individuals were informed about the objectives, procedures, potential benefits, and risks associated with the study. Adult volunteers participating in the study signed an informed consent form. A witness was required for adults who were illiterate and children who assented. Participation was voluntary, and hence, participants could withdraw at any time without further obligation.
Study area and population
The study was carried out in four departments of North Côte d’Ivoire; namely, Ouangolodougou and Ferkessédougou in the Tchologo region, and Sinématiali and Dikodougou in the Poro region (Fig 1). The North of Côte d’Ivoire is a tropical zone characterized by two seasons: the dry season, which lasts from November to March, and the rainy season from April to October. The mean annual precipitation is approximately 1,000 mm. The hydrologic system is dominated by the Bandama River and its tributaries, and several small multipurpose dams that have been constructed to enhance agricultural production and cattle rearing [21,22]. The population of the four departments was estimated at 477,000 people in 2014 [23].
The map was created with QGIS software version 2.16.0 ‘Nødebo’ (QGIS Development Team), using a basemap shapefile from the Database of Global Administrative Areas (GADM, https://gadm.org/; license: https://gadm.org/license.html).
A total of 16 villages were randomly selected, with four villages in each department. As described in a previous paper [18], these sites were chosen mainly due to the presence of human and animal schistosomiasis and the presence of small dams and water bodies frequented by both humans and livestock. An additional reason was that northern Côte d’Ivoire is the main livestock production area in the country and is an ideal site to investigate the interactions between parasites and their host species, including humans, livestock, and snails. Furthermore, in this region of Côte d’Ivoire, it is believed that elimination can be achieved, and hence, it is important to understand the transmission dynamics amongst all hosts there. People in these villages are mainly from the ethnic group of Sénoufo, but also Peulh, while there are some immigrants from neighboring countries in the North, Burkina Faso and Mali. People in this area are mainly engaged in subsidence farming (e.g., corn, rice, and vegetables). The principal cash crops are cashew nuts, cotton, and mango. Fishing is also common, mainly by non-local people in the man-made lakes.
Study design and sample size
A cross-sectional survey was carried out in August 2018 to determine the prevalence of human schistosomiasis in the study area. The estimated sample size (n) was 553 participants, based on the following formula: n = (Z2 × p (1-p) × Deff) / i2, where Z = 1.96. The expected prevalence (p) based on a previous study is 10% [24], i is the precision or margin of the error (5%-points), and Deff is the design effect (calculated as 1 + (samples per cluster—1) * intracluster correlation coefficient).
Field procedures
Recruitment of study participants.
In order to reach the sample size calculated for the departments, 50 participants were recruited per village by convenience and snowball sampling. Participants were recruited after meeting with village authorities and subsequently referred friends and family to participate. Those aged 6 years and above were invited to participate. Written informed consent was obtained at the participants’ homes, after which a questionnaire was administered to collect demographic data (e.g., age, sex, ethnicity, and education attainment), socioeconomic data, and risk factors (e.g., specific water-contact patterns). The field team provided participants with two plastic containers: one for stool and one for urine collection. The next morning, between 8:00 and 12:00 hours, the field team visited the households and collected filled containers from participants. The samples were individually labelled with a unique identification code and transferred to a nearby laboratory for parasitologic examination. In each locality, the field team was assisted by a community health worker, who was familiar with the study villages.
Snail sampling.
Concurrent to the community survey, a cross-sectional malacologic survey was conducted in waterways of the targeted localities to identify intermediate host snails of Schistosoma. Human- and animal-water contact sites were identified with the help of local guides, who were resource persons living in the selected villages. Snail sampling was carried out by two experienced field workers, who searched for and collected snails for 15 min at each site by hand using soft tweezers. In addition, a long-handed kitchen scoop was employed to reach vegetation deeper underwater and to sample collection points that were difficult to access otherwise. Upon collection in the field, the collected snails were identified to genus level and, whenever possible, to species level [25]. The snails were placed in petri dishes, between two layers of cotton wool moistened with site water and wrung out. Snails were placed with the opening against the cotton, without touching. Each dish was labelled with the name and code of the site and the date of collection. The samples were stored in a cooler with a refrigeration device to maintain the temperature between 18 and 23°C.
Laboratory procedures
Parasitologic survey.
Stool samples were analyzed using the Kato-Katz technique [26]. In brief, duplicate thick smears were prepared on microscope slides using standard 41.7 mg templates. The slides were allowed to clear for 30–45 min and were then examined under a microscope by two experienced laboratory technicians. The number of eggs of each helminth species was recorded and multiplied by a factor of 24 to obtain the number of eggs per gram (EPG) of stool.
Urine samples were subjected to a filtration method [27]. In brief, 10 ml of urine was vigorously shaken and filtered through a Nytrel filter with a 40 μm mesh size and examined under a microscope for the presence of S. haematobium eggs, which were counted by experienced laboratory technicians.
Statistical analysis
Statistical analyses were performed with Stata version 15.0 (Stata Corporation; College Station, TX, United States of America). Participants were stratified into four age groups (6–10, 11–15, 16–20, and >20 years). To account for clustering, the confidence intervals (CIs) of the overall prevalence were adjusted using a constant only, generalised estimating equation (GEE) model with robust sandwich variance estimators. For each participant, the arithmetic mean of the number of species-specific helminth egg counts was calculated based on the duplicate Kato-Katz thick smear readings. At the department level, the geometric mean egg counts were calculated. Helminth infection intensities were classified according to WHO guidelines (Table 1) [28]. Associations between parasitic infections and risk factors (e.g., sex and age) were assessed using GEE analysis for binary outcomes with village as clusters.
Results
Characteristics of the study population
A total of 742 participants aged 6–96 years from four departments in the northern part of Côte d’Ivoire were included; namely, Ouangolodougou, Ferkessédougou, Sinématiali, and Dikodougou. Males represented 59.0% of the sample, 50.4% of participants were school-age children (5–15 years), and most participants were students, housewives, and crop farmers (Table 2).
Numbers in brackets are percentages.
Schistosoma and hookworm infections
The overall prevalence of schistosomiasis was very low in the study area; 1.9% (95% CI: 0.7–5.3%) and 0.3% (95% CI: 0.1–1.0%) for S. haematobium and S. mansoni, respectively (Table 3). At the unit of the department, the prevalence of schistosomiasis was also low; the highest prevalence was observed in Ferkessédougou (5.4%, 95% CI: 2.5–9.9%), followed by Ouangolodougou (2.2%, 95% CI: 0.6–5.5%). At the unit of the village, the prevalence of schistosomiasis was low with one exception; Village C in Ferkessédougou had a moderate prevalence of 21.2% (95% CI: 9.0–38.9%). As regards STH, hookworm was the only species found with a low overall prevalence of 1.5% (95% CI: 0.8–2.8%).
Low average infection intensities of the two schistosome species and hookworm were observed in all four departments with geometric means of 16.2 eggs per 10 ml of urine (95% CI: 4.2–62.7 per 10 ml of urine) for S. haematobium, 93.0 EPG (95% CI: 0.4–24,198 EPG) for S. mansoni, and 156.5 EPG (95% CI: 52.1–470.3 EPG) for hookworm. Infection intensities were also generally low for all three parasites with over half of those infected having low infection intensities (Fig 2). However, high infection intensities were observed in those aged 11–15 years (67%) and older than 20 years (50%) for S. haematobium, and in 5- to 10-year-old children (25%) for hookworm (Fig 2).
For the definition of infection intensities, see Table 1.
Table 4 shows the association between an infection (S. haematobium and hookworm), and sex or age. S. mansoni infection was not considered in the analysis, because of the very low prevalence (2/742). Males had a higher risk of infection with S. haematobium compared to females, but the difference was not statistically significant (2.3% versus 1.3%, odds ratio [OR]: 1.5, 95% CI: 0.8–2.7). Males had higher odds of hookworm infection than females, but the difference lacked statistical significance (2.3% versus 0.3%, OR: 5.5, 95% CI: 0.6–53.7). Participants aged 16–20 years had higher odds of infection with S. haematobium than other age groups (OR: 5.3, 95% CI: 1.8–15.7), and fishermen had the highest odds of S. haematobium infection (Fig 3).
Results of malacologic surveys
A total of 111 human- and animal-water contact sites were identified at 47 water sources in the study area. The number of these contact sites ranged between 18 (Dikodougou) and 35 (Ferkessédougou). These contact sites were distributed amongst seven water sources in Sinématiali, 11 in Dikodougou, 11 in Ouangolodougou, and 18 in Ferkessédougou. Small dams (n = 22) were the most common human- or animal-water contact sites, followed by rivers (n = 13) and ponds (n = 12).
A total of 1,273 freshwater snails belonging to seven genera were collected, namely, Biomphalaria, Bulinus, Gabbiella, Gyraulus, Lanistes, Lymnaea, and Melanoides (Table 5). Bulinus forskalii (n = 761) was the most abundant snail species in the study area, consisting of over half of the snails collected. Concerning schistosomiasis, potential intermediate host snails were Bu. forskalii (NB: bring on one line; “forskalii” not capital) (n = 761), Bulinus truncatus (n = 205), and Biomphalaria pfeifferi (n = 1). From these snails, one specimen of Bu. truncatus was found to be shedding schistosome cercariae, while some snails were observed shedding several zoophilic cercariae not pathogenic to humans, namely, strigeids, echinostomes, and xiphidiocercariae (Table 6).
Discussion
In the new WHO road map, schistosomiasis and STH are targeted for elimination as a public health problem by 2030 [7]. The prevalence and risk factors of schistosomiasis and STH were assessed in four departments in the northern part of Côte d’Ivoire. Overall, a very low prevalence of S. mansoni (0.3%) and a somewhat higher, but still very low, prevalence of S. haematobium (1.9%) were found. Hookworm was the only STH observed with a very low overall prevalence (1.5%), and infection intensities were mainly low.
The observations in North Côte d’Ivoire confirm the low endemicity of schistosomiasis. Indeed, this part of Côte d’Ivoire is known to have low to moderate prevalence of schistosomiasis [16]. In 2015, a study in Korhogo noted a low prevalence of 1.9% for both urogenital and intestinal schistosomiasis among school-age children [29]. The low prevalence of schistosomiasis and STH might be explained by climatic factors and large-scale drug administration using praziquantel against schistosomiasis and albendazole against STH, which commenced in 2013 [16,17]. Of note, the increasing supply of safe drinking water in rural areas after a decade-long socio-political crisis (2002–2011) has contributed to the reduction of the population’s contact with cercarial-infested freshwater. Nevertheless, at the unit of the village, there was one study site in the department of Ferkessédougou that showed a moderate prevalence of S. haematobium (21.2%), and hence, is eligible for preventive chemotherapy with praziquantel [2]. This level of moderate endemicity is likely related to a small multipurpose dam in close proximity to the village, with which the population is in frequent contact for farming or cattle watering. Dams have long been known to be associated with an elevated risk of schistosomiasis [30–32]. Although the prevalence of schistosomiasis is low in North Côte d’Ivoire, it is worth mentioning that livestock schistosomiasis is widespread in this part of the country [18] and hybridization between S. bovis (cattle schistosome) and S. haematobium has recently been observed in humans [10,12]. The use of new and more sensitive techniques, such as molecular tools, is needed in this low-endemicity context in order to detect light-intensity infections that evade detection with the standard Kato-Katz technique [33]. When evaluating the prevalence of schistosomiasis, preschool-age children (< 6 years) that were not included in this study, should be considered in order to have a complete overview of the situation. In fact, preschool-age children may be infected when accompanying their caregivers to water bodies that are likely to be infested with schistosome cercariae [34,35]. The new formulations of praziquantel for preschool-age children is a welcome addition to the armamentarium for reducing the burden of schistosomiasis in this age group, which has not been targeted for a long time by mass drug administration campaigns [36].
The somewhat higher prevalence of S. haematobium compared to S. mansoni was also observed in previous studies [16,37]. This observation could be explained by the distribution of intermediate host snails. In fact, Bu. truncatus and Bu. globosus, two important intermediate host snails of S. haematobium, seem to be more abundant in northern Côte d’Ivoire than Bi. pfeifferi, which serves as the intermediate host snail of S. mansoni in Côte d’Ivoire. Previous research revealed that S. mansoni is the predominant schistosome species present in the West and South of Côte d’Ivoire [35,38,39].
Concerning risk factors, both males and females were exposed to S. haematobium infection. Adolescents and young adults (age range 16–20 years) were at a higher odds of being infected with S. haematobium than their younger or older counterparts. In fact, this age group might include males who fish, a high risk activity for schistosome infection because it involves frequent and prolonged contact with potentially infested freshwater sources [13,40,41]. It should be noted that high intensities of S. haematobium infection have been observed in children aged 11–15 years, reinforcing that this age group is at risk for schistosomiasis. School-age children are reported to engage in activities such as bathing and swimming in open water [13]. Furthermore, it is common practice in the study area for males aged 11–15 years to drive cattle from pasture to water at rivers and small dams. This practice frequently exposes young males to cercarial-infested water sources.
Males were at a higher odds of hookworm infection than females (OR: 5.5, 95% CI: 0.6–53.7). In our study, males were exposed to hookworm infection through activities such as farming and animal husbandry. Indeed, open defecation, a major risk factor for hookworm infection [42], is practiced on the outskirts of villages in areas that are ploughed and used for maize cultivation by adult males during the rainy season. The maize areas are abandoned and occupied by weeds in the dry season, during which time open defecation is practiced. A study in the departments of Taabo, Toumodi, and Djékanou in the south-central part of Côte d’Ivoire found that males were at a higher odds of hookworm infection than females due to the high level of open defecation on rural cocoa farms [43].
The malacologic survey confirmed the presence of Bi. pfeifferi, Bu. truncatus, and Bu. forskalii in North Côte d’Ivoire, corroborating previous findings [12,44]. However, only one specimen (0.5%) of Bu. truncatus was found to be shedding schistosome cercariae. This low infection rate in intermediate host snails is in line with the observed low prevalence of human schistosomiasis. It is not a rare phenomenon to observe a very low prevalence of schistosome cercariae shedding in natural areas. An absence of snails shedding schistosome cercariae was reported from a 3-year study assessing the dynamics of freshwater snails and schistosomiasis prevalence in school children during the construction and operation of a multipurpose dam in the central part of Côte d’Ivoire [45]. Similar results were observed from a study on characteristics of persistent hotspots of S. mansoni in western Côte d’Ivoire [46]. In contrast, a study from a Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) project assessing the molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d’Ivoire reported that only 1% (25/2,417) of both Bu. truncatus and Bu. globosus were shedding schistosome cercariae [12]. That study also showed that the snails are abundant in the dry season, but the proportion of snails shedding cercariae remains quite low in all seasons [12].
This study has several limitations that are offered for discussion. First, participants were not randomly selected; the convenience and snowball sampling method used may have selected for health conscientious individuals, leading to an underestimation of the reported infection prevalence. At the time of sampling many inhabitants were away from the villages, which significantly limited the number of people available to participate. This limits the generalizability of the results. Secondly, only single stool and urine samples were collected, and hence, infection prevalence of schistosomes and hookworm are likely to be underestimated, particularly in this low endemicity setting [47].
Conclusions
Prevalence and transmission of schistosomiasis and hookworm in the northern part of Côte d’Ivoire is very low. This calls for attempts to interrupt transmission, as has been tried in a large cluster-randomized trial over a 3-year period prior to this study [48]. Although S. haematobium transmission could not be fully interrupted, preventive chemotherapy, coupled with mollusciding, resulted in marked prevalence reduction. Longer term efforts, combining preventive chemotherapy with snail control, information, education, and communication (IEC), and improved sanitation are warranted so that the ultimate goal of elimination of schistosomiasis and hookworm in these seasonal transmission settings might be achieved.
Acknowledgments
The authors would like to thank all participants for their contribution. We are also grateful to the field work team.
References
- 1. McManus DP, Dunne DW, Sacko M, Utzinger J, Vennervald BJ, Zhou X-N. Schistosomiasis. Nat Rev Dis Primers. 2018;4: 13. pmid:30093684
- 2.
WHO. WHO guideline on control and elimination of human schistosomiasis. Geneva: World Health Organization; 2022. Available from: https://apps.who.int/iris/handle/10665/351856
- 3. WHO. Schistosomiasis and soiltransmitted helminthiases: progress report, 2020. Wkly Epidemiol Rec. 2021;48: 585–595.
- 4. GBD 2017 DALYs and HALE Collaborators. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392: 1859–1922. pmid:30415748
- 5.
WHO. Ending the neglect to attain the sustainable development goals: a global strategy on water, sanitation and hygiene to combat neglected tropical diseases, 2021–2030. Geneva: World Health Organization; 2021. Available from: https://apps.who.int/iris/handle/10665/340240
- 6. Kokaliaris C, Garba A, Matuska M, Bronzan RN, Colley DG, Dorkenoo AM, et al. Effect of preventive chemotherapy with praziquantel on schistosomiasis among school-aged children in sub-Saharan Africa: a spatiotemporal modelling study. Lancet Infect Dis. 2022;22: 136–149. pmid:34863336
- 7.
WHO. Ending the neglect to attain the sustainable development goals: a road map for neglected tropical diseases 2021–2030. Geneva: World Health Organization; 2020. Available from: https://apps.who.int/iris/handle/10665/338565
- 8. Loukas A, Hotez PJ, Diemert D, Yazdanbakhsh M, McCarthy JS, Correa-Oliveira R, et al. Hookworm infection. Nat Rev Dis Primers. 2016;2: 16088. pmid:27929101
- 9. Else KJ, Keiser J, Holland CV, Grencis RK, Sattelle DB, Fujiwara RT, et al. Whipworm and roundworm infections. Nat Rev Dis Primers. 2020;6: 44. pmid:32467581
- 10. Angora EK, Allienne J-F, Rey O, Menan H, Touré AO, Coulibaly JT, et al. High prevalence of Schistosoma haematobium x Schistosoma bovis hybrids in schoolchildren in Côte d’Ivoire. Parasitology. 2020;147: 287–294. pmid:31727202
- 11. Boon NAM, Mbow M, Paredis L, Moris P, Sy I, Maes T, et al. No barrier breakdown between human and cattle schistosome species in the Senegal River Basin in the face of hybridisation. Int J Parasitol. 2019;49: 1039–1048. pmid:31734338
- 12. Tian-Bi Y-NT, Webster B, Konan CK, Allan F, Diakité NR, Ouattara M, et al. Molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d’Ivoire. Parasit Vectors. 2019;12: 117. pmid:30890180
- 13. Angora EK, Boissier J, Menan H, Rey O, Tuo K, Touré AO, et al. Prevalence and risk factors for schistosomiasis among schoolchildren in two settings of Côte d’Ivoire. Trop Med Infect Dis. 2019;4: E110. pmid:31340504
- 14. Yapi RB, Hürlimann E, Houngbedji CA, Ndri PB, Silué KD, Soro G, et al. Infection and co-infection with helminths and Plasmodium among school children in Côte d’Ivoire: results from a national cross-sectional survey. PLoS Negl Trop Dis. 2014;8: e2913. pmid:24901333
- 15. Chammartin F, Hürlimann E, Raso G, N’Goran EK, Utzinger J, Vounatsou P. Statistical methodological issues in mapping historical schistosomiasis survey data. Acta Trop. 2013;128: 345–352. pmid:23648217
- 16. Tian-Bi Y-NT, Ouattara M, Knopp S, Coulibaly JT, Hurlimann E, Webster B, et al. Interrupting seasonal transmission of Schistosoma haematobium and control of soil-transmitted helminthiasis in northern and central Cote d’Ivoire: a SCORE study protocol. BMC Public Health. 2018;18: 186. pmid:29378542
- 17. Diakité NR, Ouattara M, Bassa FK, Coulibaly JT, Tian-Bi Y-NT, Meïté A, et al. Baseline and impact of first-year intervention on Schistosoma haematobium infection in seasonal transmission foci in the northern and central parts of Côte d’Ivoire. Trop Med Infect Dis. 2021;6. pmid:33429843
- 18. Kouadio JN, Giovanoli Evack J, Achi LY, Fritsche D, Ouattara M, Silué KD, et al. Prevalence and distribution of livestock schistosomiasis and fascioliasis in Côte d’Ivoire: results from a cross-sectional survey. BMC Vet Res. 2020;16: 446. pmid:33203412
- 19. Giovanoli Evack J, Kouadio JN, Achi L, Balmer O, Hattendorf J, Bonfoh B, et al. Accuracy of the sedimentation and filtration methods for the diagnosis of schistosomiasis in cattle. Parasitol Res. 2020;119: 1707–1712. pmid:32236710
- 20. Kouadio JN, Giovanoli Evack J, Achi LY, Balmer O, Utzinger J, N’Goran EK, et al. Efficacy of triclabendazole and albendazole against Fasciola spp. infection in cattle in Côte d’Ivoire: a randomised blinded trial. Acta Trop. 2021;222: 106039. pmid:34252386
- 21. Cecchi P. De la construction d’un objet pluridisciplinaire: les “Petits-Barrages” du nord de la Côte d’Ivoire. Nat Sci Soc. 1998;6: 73–83.
- 22. Cecchi P, Gourdin F, Koné S, Corbin D, Etienne J, Casenave A. Les petits barrages du nord de la Côte d’Ivoire: inventaire et potentialités hydrologiques. Secheresse. 2009;20: 112–122.
- 23. Institut National de la Statistique. Recensement général de la popupalion et de l’habitat 2014-Résultats globaux. Abidjan; 2016. Available from: https://www.ins.ci/documents/rgph/ivoirien18plus.pdf
- 24. Chammartin F, Houngbedji CA, Hürlimann E, Yapi RB, Silué KD, Soro G, et al. Bayesian risk mapping and model-based estimation of Schistosoma haematobium–Schistosoma mansoni co-distribution in Côte d’Ivoire. Clements ACA, editor. PLoS Negl Trop Dis. 2014;8: e3407. pmid:25522007
- 25. Frandsen F, Christensen NO. An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Trop. 1984;41: 181–202. pmid:6206702
- 26. Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972;14: 397–400. pmid:4675644
- 27. Plouvier S, Leroy JC, Colette J. A propos d’une technique simple de filtration des urines dans le diagnostic de la bilharziose urinaire en enquête de masse. Med Trop. 1975;35: 229–230.
- 28. WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Rep Ser. 2002; 912: 1–57. Available from: http://www.who.int/iris/handle/10665/42588
- 29. M’Bra RK, Kone B, Yapi YG, Silué KD, Sy I, Vienneau D, et al. Risk factors for schistosomiasis in an urban area in northern Côte d’Ivoire. Infect Dis Poverty. 2018;7: 47. pmid:29773076
- 30. N’Goran EK, Diabate S, Utzinger J, Sellin B. Changes in human schistosomiasis levels after the construction of two large hydroelectric dams in central Côte d’Ivoire. Bull World Health Organ. 1997;75: 541–545.
- 31. Sokolow SH, Jones IJ, Jocque M, La D, Cords O, Knight A, et al. Nearly 400 million people are at higher risk of schistosomiasis because dams block the migration of snail-eating river prawns. Phil Trans R Soc B. 2017;372: 20160127. pmid:28438916
- 32. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006;6: 411–425. pmid:16790382
- 33. Utzinger J, Becker SL, van Lieshout L, van Dam GJ, Knopp S. New diagnostic tools in schistosomiasis. Clin Microbiol Infect. 2015;21: 529–542. pmid:25843503
- 34. Stothard JR, Sousa-Figueiredo JC, Betson M, Green HK, Seto EYW, Garba A, et al. Closing the praziquantel treatment gap: new steps in epidemiological monitoring and control of schistosomiasis in African infants and preschool-aged children. Parasitology. 2011;138: 1593–1606. pmid:21861945
- 35. N’Zi CK, Ouattara M, Assaré RK, Bassa FK, Diakité NR, N’Goran EK. Risk factors and spatial distribution of Schistosoma mansoni infection among preschool-aged children in Blapleu, Biankouma District, Western Côte d’Ivoire. J Trop Med. 2021;2021: e6224401. pmid:34876909
- 36. N’Goran EK, Yalkinoglu Ö, Kourany-Lefoll E, Tappert A, Hayward B, Yin X, et al. Efficacy and safety of new orodispersible tablet formulations of praziquantel (Racemate and L-Praziquantel) in Schistosoma mansoni-infected preschool-age children and infants: a randomized dose-finding phase 2 study. Front Trop Dis. 2021;2: 679373.
- 37. Krauth SJ, Greter H, Stete K, Coulibaly JT, Traoré SI, Ngandolo BNR, et al. All that is blood is not schistosomiasis: experiences with reagent strip testing for urogenital schistosomiasis with special consideration to very-low prevalence settings. Parasit Vectors. 2015;8. pmid:26554822
- 38. Raso G, Matthys B, N’Goran EK, Tanner M, Vounatsou P, Utzinger J. Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Côte d’Ivoire. Parasitology. 2005;131: 97–108. pmid:16038401
- 39. Utzinger J N’Goran EK, Ossey YA, Booth M, Traoré M, Lohourignon KL, et al. Rapid screening for Schistosoma mansoni in western Côte d’Ivoire using a simple school questionnaire. Bull World Health Organ. 2000;78: 389–398.
- 40. Melo AGS de, Irmão JJ de M, Jeraldo V de LS, Melo CM. Schistosomiasis mansoni in families of fishing workers of endemic area of Alagoas. Esc Anna Nery. 2018;23.
- 41. Tukahebwa EM, Magnussen P, Madsen H, Kabatereine NB, Nuwaha F, Wilson S, et al. A very high infection intensity of Schistosoma mansoni in a Ugandan Lake Victoria fishing community is required for association with highly prevalent organ related morbidity. PLoS Negl Trop Dis. 2013;7: e2268. pmid:23936559
- 42. Loukouri A, Méité A, Kouadio OK, Djè NN, Trayé-Bi G, Koudou BG, et al. Prevalence, intensity of soil-transmitted helminths, and factors associated with infection: importance in control program with ivermectin and albendazole in eastern Côte d’Ivoire. J Trop Med. 2019;2019: 7658594. pmid:31019535
- 43. Coulibaly G, Ouattara M, Dongo K, Hürlimann E, Bassa FK, Koné N, et al. Epidemiology of intestinal parasite infections in three departments of south-central Côte d’Ivoire before the implementation of a cluster-randomised trial. Parasite Epidemiol Control. 2018;3: 63–76. pmid:29774300
- 44. Krauth SJ, Wandel N, Traoré SI, Vounatsou P, Hattendorf J, Achi LY, et al. Distribution of intermediate host snails of schistosomiasis and fascioliasis in relation to environmental factors during the dry season in the Tchologo region, Côte d’Ivoire. Adv Water Resour. 2017;108: 386–396.
- 45. Diakité NR, Winkler MS, Coulibaly JT, Guindo-Coulibaly N, Utzinger J, N’Goran EK. Dynamics of freshwater snails and Schistosoma infection prevalence in schoolchildren during the construction and operation of a multipurpose dam in central Côte d’Ivoire. Infect Dis Poverty. 2017;6: 93. pmid:28468667
- 46. Assaré RK N’Tamon RN, Bellai LG, Koffi JA, Mathieu T-BI, Ouattara M, et al. Characteristics of persistent hotspots of Schistosoma mansoni in western Côte d’Ivoire. Parasit Vectors. 2020;13: 337. pmid:32616074
- 47. Bärenbold O, Raso G, Coulibaly JT, N’Goran EK, Utzinger J, Vounatsou P. Estimating sensitivity of the Kato-Katz technique for the diagnosis of Schistosoma mansoni and hookworm in relation to infection intensity. PLoS Negl Trop Dis. 2017;11: e0005953. pmid:28976979
- 48. Ouattara M, Bassa FK, Diakité NR, Hattendorf J, Coulibaly JT, Yao PK, et al. Effectiveness of four different interventions against Schistosoma haematobium in a seasonal transmission setting of Côte d’Ivoire: a cluster randomized trial. Clin Infect Dis. 2022;74: 2181–2190. pmid:34519344