Epidemiology, spatial distribution and control of schistosomiasis mansoni in western Côte d'Ivoire

Summary
Background: Preventive chemotherapy is a strategy of delivering anthelmintic drugs to people at-risk of schistosomiasis without prior diagnosis. Currently, World Health Organization (WHO) recommends this strategy for morbidity control targeting six major helminthiases among the 17 neglected tropical diseases (NTDs) which pose a considerable public health problem and impair the economic development of tropic and sub-tropical countries. Among these helminthiases, schistosomiasis affects more than 250 million people, mainly in sub-Sahara Africa. Since the mid-1980s, preventive chemotherapy with praziquantel has been advocated by WHO for schistosomiasis control. It is believed that high-coverage of preventive chemotherapy in endemic settings not only prevents morbidity and long-term sequelae of schistosomiasis, but might also interrupt the transmission of the disease. The present WHO goal for schistosomiasis morbidity control is to regularly reach at least 75% and up to 100% of school-aged children in endemic areas. This ambitious target was supported by international donors and pharmaceutical companies who decided to offer praziquantel tablets free of charge to endemic countries. While, preventive chemotherapy with praziquantel is being scaled up there are several concerns, such as treatment failure to clear infection, development and spread of drug resistance, low drug coverage particularly after several years of administration, lack of baseline data for better assessment of the treatment impact and sustainability of this strategy.
Goal and specific objectives: The overarching goal of this Ph.D. thesis was to deepen our understanding of the epidemiology and spatial distribution of schistosomiasis mansoni in four regions of western Côte d’Ivoire, and to assess the impact of preventive chemotherapy with praziquantel on schistosomiasis one-year post-treatment. The study was readily integrated into a multi-country investigation financed by the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE). This thesis pursued four specific objectives. First, to contribute to the design of a study protocol with the aim to sustain the control of Schistosoma mansoni in moderate endemicity areas (prevalence of infection of baseline: 10-24%). Second, to map and predict the spatial distribution of S. mansoni in the western part of Côte d’Ivoire. Third, to determine the baseline parasitological and social-ecological situation of local communities before the implementation of a randomised controlled trial to sustain schistosomiasis mansoni control. Fourth, to assess the impact of preventive chemotherapy with praziquantel on the prevalence and intensity of S. mansoni and to determine the dynamics of infection one year after the treatment intervention.
Methods: The field work for this Ph.D. was split into three parts: eligibility, baseline and one-year post-treatment surveys. The eligibility survey took place from June to August 2011 and in December 2011. School-based cross-sectional parasitological surveys were conducted in Cavally, Guemon, Tonkpi, and Haut-Sassandra, regions of western Côte d’Ivoire. Around 50 children aged 13-14 years per school were screened for S. mansoni infection using duplicate Kato-Katz thick smears. 75 schools with S. mansoni prevalence ranging between 10% and 24% were selected for a more detailed baseline survey and randomised to one of three treatment arms (A, B and C). Baseline surveys were carried out from December 2011 to February 2012. Approximately 100 children aged 9-12 years per school provided three stool samples on three consecutive days, while a single stool sample was collected from 100 first graders. The stool samples were subjected to the Kato-Katz method (duplicate Kato-Katz thick smears per stool sample) for identification and enumeration of S. mansoni eggs. In addition, a questionnaire on socio-demographic and ecological factors that might influence S. mansoni transmission was delivered to school directors and village leaders. In June 2012, a combined school- and community-based mass drug administration with praziquantel (single dose of 40 mg/kg) was conducted, targeting school-aged children living in the school catchment areas. Praziquantel treatment was delivered to children by trained school teachers. In May 2013, One-year post-treatment, a survey was conducted in the 50 schools of treatment arms A and B. Approximately, 100 children aged 9- 12 years per school were screened on three consecutive days for S. mansoni infection using the Kato-Katz method. The prevalence and intensity of S. mansoni infection were compared between the baseline and the one-year follow-up surveys at the respective schools.
Results: At the eligibility survey, 264 schools were screened. The overall prevalence of S. mansoni was 39.9%, ranging from 0% to 100% at the unit of the school. High S. mansoni prevalence rates were mostly observed in Tonkpi region. Overall, 157 (59.5%) schools had prevalence of S. mansoni above 24%, 78 (29.5%) schools had a prevalence ranging between 10% and 24%, while the remaining 29 schools (11.0%) showed prevalences below 10%. Bayesian geostatistical analysis showed that age, sex, altitude and difference between land surface temperature at day and night were significantly correlated with S. mansoni infection. Rice cultivation, open defecation, use of traditional pit latrine, use of natural open freshwater bodies for washing and bathing were potential risk factors associated with S. mansoni in local communities. At the baseline survey, after considering at least quadruplicate Kato-Katz thick smears per child, among the 75 schools where the prevalence of S. mansoni was moderate in the eligibility survey (10-24%) we found that the prevalence of infection was higher than 24% in 28 schools (37.3%), while it was below 10% in 7 schools (9.3%). At treatment arm level, we found that the S. mansoni prevalence of treatment arm C was slightly higher compared to arms A and B. Our data showed that the directly observed treatment coverage was 84.2%. At the unit of the school, we found that coverage of ≥75% was achieved in 57 schools (76.0%). One year post-treatment, the overall prevalence of S. mansoni in the 50 schools of treatment arms A and B decreased from 19.7% to 12.8%, while the intensity of the infection slightly increased from 94.9 eggs per gram of stool among infected children to 109.3 eggs per gram of stool. The dynamics of prevalence and intensity of S. mansoni were heterogeneous.
Conclusion: The understanding of the spatial distribution of schistosomiasis can help decision-makers for better planning disease control. In the frame of this Ph.D., a spatial explicit risk map of S. mansoni was generated for the western part of Côte d’Ivoire that was already been used by the national control programme for spatial targeting of control interventions. In addition, the study showed that the classification of communities according to WHO guideline is fragile which calls for a more accurate tool of categorisation of communities based on the schistosomiasis endemicity. The baseline parasitological and social-ecological situation in the villages provided important information for the 4-year cluster-randomised intervention trial founded by SCORE, which will help to determine the best strategies to sustainably control schistosomiasis mansoni. Our results demonstrated that the dynamics of schistosomiasis in the study areas one-year post-treatment was heterogeneous. Thus, on one hand, there is a need to regularly assess the dynamics of schistosomiasis during this SCORE study to deepen our understanding of the dynamics of schistosomiasis transmission, while on the other hand it might be necessary to implement more integrated control interventions to sustain gains made by preventive chemotherapy and more from morbidity control to elimination.