Research Article: Assessing the benefits of five years of different approaches to treatment of urogenital schistosomiasis: A SCORE project in Northern Mozambique

Date Published: December 8, 2017

Publisher: Public Library of Science

Author(s): Anna E. Phillips, Pedro H. Gazzinelli-Guimaraes, Herminio O. Aurelio, Josefo Ferro, Rassul Nala, Michelle Clements, Charles H. King, Alan Fenwick, Fiona M. Fleming, Neerav Dhanani, Peter Steinmann.

Abstract: BackgroundIn Mozambique, schistosomiasis is highly endemic across the whole country. The Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) coordinates a five-year study that has been implemented in various African countries, including Mozambique. The overall goal of SCORE was to better understand how to best apply preventive chemotherapy with praziquantel (PZQ) for schistosomiasis control by evaluating the impact of alternative treatment approaches.MethodsThis was a cluster-randomised trial that compared the impact of different treatment strategies in study areas with prevalence among school children of ≥21% S. haematobium infection by urine dipstick. Each village was randomly allocated to one of six possible combinations of community-wide treatment (CWT), school-based treatment (SBT), and/or drug holidays over a period of four years, followed by final data collection in the fifth year. The most intense intervention arm involved four years of CWT, while the least intensive arm involved two years of SBT followed by two consecutive years of PZQ holiday. Each study arm included 25 villages randomly assigned to one of the six treatment arms. The primary outcome of interest was change in prevalence and intensity of S. haematobium among 100 children aged 9-to-12-years that were sampled each year in every village. In addition to children aged 9-to-12 years, 100 children aged 5–8 years in their first-year of school and 50 adults (aged 20–55 years) were tested in the first and final fifth year of the study. Prevalence and intensity of S. haematobium infection was evaluated by two filtrations, each of 10mL, from a single urine specimen.Principal findingsIn total, data was collected from 81,167 individuals across 149 villages in ten districts of Cabo Delgado province, Northern Mozambique. Overall PZQ treatment resulted in a significant reduction in the prevalence of S. haematobium infection from Year 1 to Year 5, where the average prevalence went from 60.5% to 38.8%, across all age groups and treatment arms. The proportion of those heavily infected also reduced from 17.6% to 11.9% over five years. There was a significantly higher likelihood of males being infected than females at baseline, but no significant difference between the sexes in their response to treatment. The only significant response based on a study arm was seen in both the 9-to-12-year-old and first-year cross sections, where two consecutive treatment holidays resulted in a significantly higher final prevalence of S. haematobium than no treatment holidays. When the arms were grouped together, four rounds of treatment (regardless of whether it was CWT or SBT), however, did result in a significantly greater reduction in S. haematobium prevalence than two rounds of treatment (i.e. with two intermittent or consecutive holiday years) over a five-year period.ConclusionsAlthough PC was successful in reducing the burden of active infection, even among those heavily infected, annual CWT did not have a significantly greater impact on disease prevalence or intensity than less intense treatment arms. This may be due to extremely high starting prevalence and intensity in the study area, with frequent exposure to reinfection, or related to challenges in achieving high treatment coverage More frequent treatment had a greater impact on prevalence and intensity of infection when arms were grouped by number of treatments, however, cost efficiency was greater in arms only receiving two treatments. Finally, a significant reduction in prevalence of S. haematobium was seen in adults even in the SBT arms implying the rate of transmission in the community had been decreased, even where only school children have been treated, which has significant logistical and cost-saving implications for a national control programme in justifying CWT.

Partial Text: Schistosomiasis is a major yet neglected public health problem, second only to malaria in terms of parasite-induced human morbidity and mortality worldwide [1]. Estimates show that globally at least 218 million people required preventive treatment in 2015 [2–4], and at least 20 million suffer from severe and debilitating forms of the disease [5]. Schistosomiasis is a major public health problem in Mozambique, as shown by an epidemiological survey of schistosomiasis and soil-transmitted helminthiasis among school children carried out between 2005 and 2007 [6]. The mean estimated prevalence of urogenital schistosomiasis, Schistosoma haematobium, was 47% while that of intestinal schistosomiasis, S. mansoni, was much lower (around 1%) across all of Mozambique. In Cabo Delgado province, the area where this study took place, the prevalence of S. haematobium was 57.9%, ranging from 8.8% on the coast to 93% inland [6].

Data were collected in the dry season between July and October each year from 2011 until 2015 in ten districts of Cabo Delgado province, Northern Mozambique. It was intended to sample 105,000 people from a total of 150 villages over the five years, but due to poor school enrolment and absence from many villages by children and adults working in the fields and mines, our final analysis included 81,167 individuals (77.3% participation). One village dropped out of the study prior to data collection due to political issues, therefore data is available from 149 villages.

In Cabo Delgado, Mozambique, S. haematobium infection was found prevalent throughout all 149 schools in the study, where many schools had 90% baseline prevalence (Fig 2). The primary outcome of the study was to examine the change in infection among 9-to-12-year olds between specified study arms. Our findings showed a significant decrease in S. haematobium infection in this age group from a mean prevalence of 66.4% in Year 1 (of which 22.5% were heavily infected) to 42.5% in Year 5 (when 13.4% were heavily infected). When comparing the impact of treatment strategy each year, the only significant response to study arm was seen between annual SBT (arm 4) and two years of SBT followed by two consecutive treatment holidays (arm 5), which resulted in a higher final prevalence than when there were no treatment holidays. There were no significant differences in Year 5 prevalence for the other treatment comparisons. The general uptrend in prevalence and intensity of S. haematobium infection shown after two subsequent holiday years, compared with one-year post-treatment, demonstrates rebound of S. haematobium if PC is interrupted. These findings of significant risk for re-emergence of infection if treatment is suspended supports previous schistosome infection modelling [30, 31].