Background The Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) coordinated a five-year study implemented in several countries, including Niger, to provide an evidence-base for programmatic decisions regarding cost-effective approaches to preventive chemotherapy for schistosomiasis control.

Methods This was a cluster-randomised trial investigating six possible combinations of annual or biannual community-wide treatment (CWT), school-based treatment (SBT), and holidays from mass treatment over four years. The most intense arm involved two years of annual CWT followed by two years of biannual CWT, while the least intensive arm involved one year of annual SBT followed by a year without treatment and two more years of annual SBT. The primary outcome of interest was prevalence and intensity of S. haematobium among 100 children aged 9-to-12-years sampled each year. In addition, 100 children aged 5-to-8 years in their first year of school and 50 adults (aged 20-to-55 years) were tested in the first and final fifth year of the study.

Results In total, data was collected from 167,500 individuals across 225 villages in nine districts within the Niger River valley, Western Niger. Overall, prevalence of S. haematobium decreased from baseline to Year 5 across all study arms. The relative reduction of prevalence was greater in biannual compared with annual treatment across all arms, however, the only significant difference was seen in areas with a high starting prevalence. Although adults were not targeted for treatment in SBT arms, a statistically significant decrease in prevalence among adults was seen in moderate prevalence areas receiving biannual (10.7% to 4.8%) SBT (p<0.001). Adults tested in the annual SBT group also showed a decrease in prevalence between Year 1 and Year 5 (12.2% to 11.0%), but this difference was not significant.

Conclusions These findings are an important consideration for schistosomiasis control programs that are considering elimination and support the idea that scaling up the frequency of treatment rounds, particularly in areas of low prevalence, will not eliminate schistosomiasis. Interestingly, the finding that prevalence decreased among adults in SBT arms suggests that transmission in the community can be reduced, even where only school children are being treated, which could have logistical and cost-saving implications for the national control programmes.

Human schistosomiasis is an acute and chronic, water-associated parasitic disease that remains a major public health problem in sub-Saharan Africa. It represents the second most endemic parasite after malaria in these regions [1]. According to the World Health Organisation (WHO), an estimated 218 million people need preventive chemotherapy (PC) worldwide, of which 92% live in Africa [2].

It is estimated that 3.2 million people are infected with schistosomiasis in Niger [3]. Both Schistosoma haematobium and Schistosoma mansoni are endemic, but the main species is S. haematobium, which is distributed in all regions of the country [4]. Previously S. mansoni had a relatively marginal role, however, more recently an increase in infection has been seen in the western part of the Niger River Valley. A national program for the control of schistosomiasis and geohelminthiasis was implemented by the Niger Ministry of Health in 2004 [5]. The control strategies used were school-based treatment (SBT) with praziquantel (PZQ) to reduce morbidity caused by schistosomiasis, and selective chemotherapy in adults at high risk of infection, following the WHO guidelines [6–7].

Previously, a combined school- and community-based strategy has been shown to be effective in attaining a high coverage among school-age children (SAC) in countries where school enrolment is low and where primary schools cannot serve as the exclusive drug distribution points [8–11]. Furthermore, there is a growing body of evidence regarding the burden of infection in adults and their potential role in sustaining transmission, which suggests a need for them to be included in treatment programmes [11–16].

Whether community-wide treatment (CWT) is appropriate depends on the local epidemiological setting and whether the goal is morbidity control or eliminating transmission [17]. Some studies, for example, have found that SBT and community-wide treatment (CWT) yielded a similar prevalence decrease [18–19]. There is also debate around the optimal frequency of PZQ treatment for infection and morbidity control; some studies have found that the more frequent the PC, the greater impact on parasite control [20], while others have shown that a single dose of PZQ results in sustained low transmission of S. haematobium for two years [21]. In light of the controversy around the optimal approach to drug-based control of schistosomiasis, the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) was established in 2008 to address this and other questions of practical significance. An important part of SCORE’s portfolio was multi-country field studies, which included Niger, that have evaluated the impact of alternative approaches to PC through CWT, SBT, and years without mass drug administration (MDA) [22].

The SCORE protocol and baseline characteristics of study populations have been described elsewhere [22–24]. In brief, SCORE projects include “Gaining control of schistosomiasis” studies, evaluating PC in communities with high prevalence of schistosomiasis, and “Sustaining control of schistosomiasis” studies, examining PC in areas of moderate schistosomiasis prevalence [22].

In 2011, SCORE began supporting Niger to conduct both “Gaining” and “Sustaining” S. haematobium control studies in two separate parts of the Niger River Valley. A simple random allocation approach was supposed to have been used to assign all eligible villages to study arms. Instead, during the selection of the field sites, Niger geographically clustered groups of villages into study arms. Following Year 2 of the study, when this was recognised, the Niger study was redesigned to compare annual versus biannual SBT or CWT. An additional deviation from the SCORE protocol included replacing the treatment ‘holiday’ years with a test-and-refer strategy, whereby mass drug administration was not given on these years, but individuals were tested and those found to be positive were referred to health centres for treatment.

The primary research question presented here is which PC strategy provided the greatest reduction in prevalence and intensity of S. haematobium infection among 9-to-12-year olds after four years of intervention. In addition, the impact of treatment on first-year students and adults was also assessed.

The SCORE project commenced in Niger with the goal of providing an evidence base for programmatic decisions on how best to control urogenital schistosomiasis, and ultimately eliminate the public health problem in both highly and moderately endemic areas. Depending on the prevalence of schistosomiasis infection in a given community, WHO recommends PC using either a school-based or community-wide approach [7]. The initial aim of this study was to examine the impact of SBT, CWT and treatment holidays for the control of S. haematobium in villages with both a high (⩾21%) and moderate (10–24%) prevalence. In Year 3 the study was redesigned, however, to compare annual versus biannual treatment delivered by either SBT or CWT.

The primary research question presented here is which PC strategy provided the greatest reduction in prevalence and intensity of S. haematobium infection among 9-to-12-year olds after four years of intervention in the Niger River Valley. Biannual SBT treatment was found to be significantly more effective for reducing active schistosome infection than annual SBT in high prevalence areas (Arm B1 vs. B2). There was no significant effect of treatment frequency, however, in areas with a low starting prevalence (Arm A1 vs. A2), or in higher prevalence areas receiving CWT (Arm C1 vs. C2).

Although the purpose of the eligibility survey was to ensure a high enough starting prevalence to make comparisons between treatment arms, the eligibility survey did have higher infection rates than the baseline parasitological survey whereby several villages had high enough prevalence using Hemastix® but when assessed by urine filtration the prevalence was lower than 10% (see Table 5 in Appendix). Some studies have shown that in very low prevalence settings, microhaematuria can be an unstable proxy for urogenital schistosomiasis [29–30]. On the other hand, the sensitivity of microscopic egg detection can vary according to intensity of infection, day-to-day variation in egg secretion, time the sample was collected, and number of examined samples [31–35]. Another potential reason for the difference in dipstick and microscopic examination could be the fact that the eligibility was carried out in 13-to-14-year olds and the parasitology survey among 9-to-12-year olds. Some studies have shown that 13-to-14-year olds harbour higher infection levels due to them not attending school and therefore more likely to be exposed to infection [36]. Other studies have showed that many cases of urogenital schistosomiasis stay undetected when the examination method is limited to urine filtration [37–38].

Both age and gender influenced infection with these findings supported by that of other studies, which have shown that the highest prevalence and intensities of infection occurred in males and among older adolescents, with infection decreasing in adulthood [36, 39–40]. There was no significant difference, however, in response to different treatment approach by age and sex.

To evaluate the potential longer-term impact of the program, we also examined the infections in first-year students, some of whom had not received treatment previously in SBT communities as they had only recently started attending school. It is important to note that S. haematobium infection in this group of children decreased significantly over four rounds of treatment, implying that the level of environmental transmission in these areas could have been reduced because of overall reductions in excreted eggs from infected children.

Currently the justification for targeting adults in a schistosomiasis control programme is based on the prevalence of infection in SAC [7]. A study in Nigeria, however, has shown that monitoring and evaluation of activities based on SAC was not a successful indicator of the burden of infection in adults [41]. The burden in adults will likely be driven by many local behavioural and cultural factors, and is, therefore, context specific. This makes it difficult to make a universal SAC infection prevalence threshold for switching to CWT. For this reason, adults were also sampled in this study. The findings here demonstrated that biannual CWT was not significantly more effective at reducing prevalence and intensity of infection. This lack of statistical significance, however, may be attributed to the difference in starting prevalence of the two groups whereby Group C1 was 14.3% and C2 was 23.4%. An important reason why studies find contrasting results regarding the benefit of CWT is the variation in the relative worm burden harboured by adults across different geographical settings; indeed, it has been modelled by Turner et al that the higher the pre-control burden in adults, the larger the benefit of switching to CWT [13]. Interestingly, there was a significant reduction in prevalence of S. haematobium infection seen among adults even in Group B implying the rate of transmission in the community had been decreased, even where only school children have been treated. These findings of reduction in infection among adults even in SBT communities was also seen in Mozambique [42].

Research in Niger has shown that the full economic delivery cost of SBT in 2005/06 was $0.76 and CWT was $0.46. Including only the programme costs the figures were $0.47 and $0.41 respectively [43]. Differences at sub-district were more marked. This is partly explained by the fact that a CDD treats 5.8 people for every one treated in school [43]. Although CWT did show a significant impact on the prevalence and intensity of S. haematobium infection among adults, given that prevalence also decreased among adults in SBT areas and twice-yearly CWT did not have a significantly greater impact on prevalence reduction with respect to annual CWT, these findings both have significant logistical and cost-saving implications for a national control programme and the justification for CWT.

The success of PC programmes may be influenced by a wide range of factors such as initial levels of endemicity and transmission intensities in the local environment; treatment frequency, coverage and compliance, among others [44]. Coverage data among different age groups is an important key determinant for achieving programme targets. Although average treatment coverage in the Niger SCORE programme has been shown to be well above the recommended WHO 75% threshold, in some areas it was above 100% and therefore implies an unreliable denominator. There may have been other external issues that might have affected the success of the biannual treatment. For example, there may have been a considerable gap between coverage and compliance [45]. Even when the proportion of eligible people who received tablets reach a significant fraction of the target population (coverage), those ingesting all the tablets at the same time (compliance) may be a better indicator of how well PC is being implemented. In this study, SBT was directly observed as the survey teams were present in the schools during the treatment. For CWT, however, there is less of a guarantee that the CDD supervised actual consumption of the treatment. In addition, frequent migration of people particularly among fishing communities or the nomadic Peule communities, some of whom move between neighbouring countries, remain significant hurdles to the successful implementation of the control program, particularly in terms of ensuring repeated treatment. Finally, there was an increase in prevalence seen across all Groups in Year 3. This is likely the consequence of severe flooding across the country in 2012, which would have increased water contact as well as affecting the snail population, in addition to subsequent migration.

There were limitations to the study. One of which was the treatment coverage, as discussed above, particularly where SAC numerators were higher than SAC denominators where adults who presented for treatment at the school were registered in the MDA. The other limitation was the differential in time periods between MDAs and parasitological surveys, which were not conducted precisely at once and six-monthly time points due to the logistical challenge of conducting such large surveys and treatment in such a short time frame. It is not clear whether this contributed to the findings as it was difficult to account for this in the analysis.

Given that there is a shifting emphasis towards transmission elimination by WHO, the findings here show that with good coverage biannual SBT may be the best strategy for schistosomiasis control in high prevalence areas. In low transmission settings, however, the lack of statistical impact of two rounds of treatment indicate that it may not be possible to break transmission using through PC alone and using other strategies such as health education, WASH, and snail control, should also be considered [46, 47].

The rationale behind biannual treatment was to reduce further the prevalence and intensity of infection, meaning a greater impact on schistosomiasis control. We conclude that twice yearly SBT treatment was effective in reducing S. haematobium in high prevalence areas, with average reported high treatment coverage. Biannual SBT in low prevalence settings and CWT in high prevalence areas did not have a significant impact on infection levels, therefore we conclude that it might not be cost effective to treat biannually in such areas but to focus on more targeted treatment in persistent hot spot areas, where infection remains high despite years of treatment. Finally, there was a significant reduction in prevalence observed in non-targeted age groups in the SBT communities. This suggests that SBT has an impact at reducing transmission potential in the community. The effect this has on adults and other non-targeted age groups should be investigated further as there would be significant cost implications in maintaining SBT strategies only.

Acknowledgments

We are grateful to the members of SCORE secretariat and advisory committee for reviewing our study, their advice, input, and support of our work. We are grateful to the Schistosomiasis Control Initiative for providing praziquantel for the study, through the donation to the Ministry of Health in Niger. We thank the technicians for their support in the field and the laboratory. We are grateful to the health, education and village authorities of all districts for their contribution. Finally, we thank all the children, parents, teachers and village leaders who participated in this study.

Ethics approval and consent to participate

National and local health, educational and administrative authorities were comprehensively informed of the study. Prior to the start of the study in each village, open public meetings were carried out in the local language followed by question and answer sessions with the survey team. The purpose of the study was explained to all schoolchildren, and verbal consent was obtained from the children themselves. It was explained that any child had the chance to withdraw from the study at any point, without any consequence. Written informed consent was also obtained from school headmasters. Due to the high rate of illiteracy among these communities, finger-print consent was obtained from all participants and parents or legal guardians of the children. Ethical review of the protocol was obtained from the National Bio-ethical Committee for Health of Niger and the survey was conducted according to NBCHM guidelines (ref: IRB00002657). The study protocol was also approved by Imperial College London (ref: ICREC_10_8_2). In addition to these, the University of Georgia institutional review board IRB implemented an administrative human subjects review and issued additional approval 10533-0 for Niger.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Funding

This research was financially supported by the Bill & Melinda Gates Foundation through the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) based at the University of Georgia in Athens, United States of America, Grant RR374–053/4893196. Praziquantel tablets for schistosomiasis treatment are donated by the Schistosomiasis Control Initiative Foundation (SCIF), United Kingdom.

Availability of data and materials

The datasets used and analysed during this study are available from the corresponding author upon reasonable request.

Contributions

AEP was responsible for the formulation of the overarching research aim of the manuscript. AEP and NAD were responsible for the data curation and analysis. AEP, AG and AF were responsible for the funding acquisition. ZT, BS, IG, BS, AGN, BM, OA, HS, KMH, RA, and AAH were responsible for the investigation and data collection. AEP, AG and AAH provided the resources for the study and were involved in the overall administration of the project. AEP wrote the paper. All authors read and approved the final manuscript.

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