Two-year impact of single praziquantel treatment on infection in the national control programme on schistosomiasis in Burkina Faso
Seydou Touré a, Yaobi Zhang b, Elisa Bosqué-Oliva b, Césaire Ky a, Amado Ouedraogo a, Artemis Koukounari b, Albis F Gabrielli c, Bertrand Sellin d, Joanne P Webster b, Alan Fenwick b
Two main forms of human schistosomiasis or bilharzia exist in Africa – urinary schistosomiasis caused by Schistosoma haematobium infection and intestinal schistosomiasis caused by Schistosoma mansoni infection. There are around 165 million people in sub-Saharan Africa with the disease: about 112 million with urinary schistosomiasis and about 54 million with intestinal schistosomiasis.1–3 The mainstay of the current strategy recommended by WHO against schistosomiasis is morbidity control through preventive chemotherapy with praziquantel (PZQ).4,5 Schistosome morbidity is mainly caused by eggs trapped in various parts of the human body, depending on the species of schistosomes, hence the fundamental aim of morbidity control is to reduce intensity of infection by drug treatment. Several national control programmes on schistosomiasis and soil-transmitted helminthiasis (STH) are now being implemented across sub-Saharan Africa with financial and technical support from the Schistosomiasis Control Initiative.6–8 We have previously reported the successful implementation of the national control programme on intestinal schistosomiasis and STH using annual treatment strategy through school-based drug delivery for schoolchildren and community-based drug delivery for adults at high risk, and the great impact achieved on reducing morbidity and infection in Uganda in eastern Africa.9,10 We now report the impact of biennial treatment strategy on urinary schistosomiasis through both school- and community-based drug deliveries for school-age children in Burkina Faso in western Africa.
Burkina Faso is a land-locked country in western Africa with a total population of about 13 million, of which approximately 3.65 million are school-age children.11 S. haematobium is the main species prevalent throughout the country with focal prevalence of up to 100%, while S. mansoni is present mainly in the southern and western regions.12 Some small-scale control activities with treatment had taken place in some areas in the past,11,13 but the national control programme did not start until 2004. Full national coverage of treatment was achieved in 2005. A total of more than 3.3 million school-age children received their first treatment, representing 90.8% of the estimated school-age population in the country.11 Our results at one year post-treatment showed that treatment significantly reduced infection and morbidity by S. haematobium.14 The current paper presents the parasitological impact of a single treatment on schistosomiasis 2 years after treatment.
National control programme
Details about the national schistosomiasis control programme supported by the Schistosomiasis Control Initiative were described elsewhere.7,11 The control strategy adopted by the Ministry of Health was modified from the WHO guidelines and involved treatment once every two years to all school-age children (5–15 years old).4,5 Synergistic treatment for STH was also given to those who received treatment for schistosomiasis. The first treatment with PZQ and albendazole was implemented during 2004 and 2005 in a staggered two-phased campaign. Due to the low school enrolment rate in Burkina Faso, treatment was carried out both through schools and communities targeting school-age children not attending school. As described previously,11 the treatment campaign was coordinated and supervised by the Ministry of Health staff, involving education authorities and local communities. A specific national ‘treatment week’ was designated in October each year and health personnel at each level (regional, district and dispensary) were mobilized. Drug delivery in schools was carried out by trained school teachers. To reach non-enrolled children, health workers and community drug distributors formed fixed units at dispensary and mobile units that visited villages or hamlets seeking school-age children not attending school. Treatment against schistosomiasis was delivered using the WHO dose pole method for PZQ (600 mg tablets).15 A single dose of albendazole (400 mg) was used against STH.
Monitoring survey design
The monitoring survey was carried out among enrolled schoolchildren in selected schools due to logistic reasons. For the longitudinal surveys, sample size calculation and cohort design have been described elsewhere.14,16 Briefly, overall sample size was calculated with an expected reduction of 70% in mean intensity for S. haematobium over a 2-year period using the EpiSchisto software tool (available at: http://www.schoolsandhealth.org). An overall drop-out rate of 40% over the course of the monitoring period was also allowed. Sentinel schools were randomly selected from all schools in four priority regions targeted in 2004. Within each school, 180 children were selected randomly from each of the 7-, 8- and 11-year-old groups with approximately equal numbers of boys and girls in each age group. However, due to number and gender restrictions in each age group in each school, the actual age range was expanded to 6–14 years. Where the total number was not met in one school, the closest school with the same ecological conditions was selected. As a result, a cohort of 1727 schoolchildren was randomly selected at baseline from 16 schools. The cohort children were examined at baseline and followed up 1 year post-treatment (in 2005) and 2 years post-treatment (in 2006). At each follow-up, additional seven-year-old first-year new students (approximately 10 boys and 10 girls) from each sentinel school were randomly selected and examined. These children were expected to have been targeted for treatment through the community-based drug delivery before they joined the schools. Infection status in these children should represent the quality of community-based treatment.
In addition to the cohort follow-up, a cross-sectional survey was conducted during the second follow-up (2 years post-treatment), in which a group of children (7–14 years old) outside the original cohort were randomly selected and examined in the sentinel schools. The number, age and sex structures were matched to those in the cohort who were present at the second follow-up in each school. Infection status in these children should represent the quality of treatment in children outside cohorts in schools, to confirm and validate the cohort data, i.e. no preferred treatment was given to cohort children.
Parasitic infection status of each child was determined by parasitological examinations. Crosschecking was carried out for quality control. Monitoring activities received ethical clearance from the National Health System Local Research Ethics Committee of St Mary’s Hospital, London, as well as approval from the Ministry of Health of Burkina Faso. Written informed consent was obtained from head teachers at each school with prior agreements from parents or guardians.
One urine specimen was collected from each child to determine S. haematobium infection using the filtration method and microscopy. Generally, specimens were collected around noon (between approximately 10:00 and 13:00), 10 ml of urine was filtered through a nylon filter (pore size 12 μm, Millipore, United Kingdom) and the number of eggs counted under a microscope. For specimens of less than 10 ml, the volumes were measured before filtration and the number of eggs per 10 ml calculated. Intensity of S. haematobium infection was expressed as number of eggs per 10 ml of urine (e/10 ml).
A single stool sample was collected from each child. Duplicate Kato–Katz slides were prepared from each sample and examined on the same day to determine S. mansoni infections. Eggs were counted and individual intensity of infection was expressed as eggs per gram of faeces (epg) calculated as the arithmetic mean of the two individual slide counts. Due to logistical reasons, at the baseline survey, only around half of cohort children were randomly selected and examined by the Kato–Katz method.
Of 1727 schoolchildren recruited at baseline, 763 were successfully traced and re-examined at both follow-ups with three complete sets of longitudinal parasitological data on S. haematobium. Children who dropped out or missed either of two follow-up surveys were not included in the longitudinal analysis. Baseline characteristics of children successfully followed-up showed that they had a lower mean age (9.6 years versus 11.0 years; P < 0.01), a lower proportion of boys (54.1% versus 59.1%; P < 0.05), higher S. haematobium prevalence (59.9% versus 53.1%; P < 0.01) but a similar intensity of S. haematobium infection (93.3 e/10 ml versus 91.2 e/10 ml; P > 0.05), compared with those who had dropped out. Among 763 children, 322 had valid data entry for S. mansoni at all three surveys. These longitudinal data, together with cross-sectional analysis of three sets of data from the 7-year-old children and two sets of data from the 7–14-year-olds, are presented in this paper. Baseline data from the original cohort, including those who dropped out during the follow-ups, served as the baseline data in the two cross-sectional analyses. Result tables together with 95% confidence intervals (CI) were obtained using software SAS version 9.1 (SAS Institute, Cary, NC, United States of America). Arithmetic mean intensity of infections was used in the analysis.17,18 For longitudinal cohort data the differences were tested using the McNemar’s test for prevalence and the Wilcoxon signed rank-sum test for mean intensities. For cross-sectional analysis the |² test was used to compare differences in prevalence and the Kruskal–Wallis test to compare differences in mean intensities.
S. haematobium infection
Longitudinal cohort data
Table 1 summarizes the parasitological results from 763 cohort children successfully examined at baseline, 1 year post-treatment and 2 years post-treatment. One round of mass PZQ treatment significantly reduced prevalence in the cohort children from 59.6% at baseline to 6.2% at 1 year post-treatment and, importantly, remained at 7.7% 2 years post-treatment, an overall 87.1% reduction over 2 years (P < 0.01). The overall intensity of infection was significantly reduced from 94.2 e/10 ml at baseline to only 1.0 e/10 ml at 1 year post-treatment and 6.8 e/10 ml at 2 years post-treatment, an overall reduction of 92.8% over 2 years (P < 0.01). Significant reduction in both prevalence and intensity of infection was found in all four regions and in both boys and girls (P < 0.01; Table 1). Importantly, before treatment the proportion of heavy infections (≥ 50 e/10 ml) accounted for over 25% of the schoolchildren examined (Fig. 1). This decreased to just 0.4% at 1 year post-treatment and remained below 2% at 2 years post-treatment.
Fig. 1. Changes in the category of intensity of Schistosoma haematobium infection in schoolchildren (n=763): 3-year longitudinal data
Table 1. Schistosoma haematobium prevalence and intensity of infection in the longitudinal cohort children before and after treatmenta
These data were compared with those of baseline children with the same ages (7–14 years old) in the original cohort before treatment. Two years after treatment, overall prevalence and intensity of S. haematobium infection were significantly lower than those at baseline by 77.4% and 80.3% respectively (P < 0.01). Significant reduction in both prevalence and intensity of infection was shown in all four regions and in both boys and girls (P < 0.01; Table 2). As in the cohort data, the proportion of heavy infections was reduced from 25% to just 3.2% (Fig. 2). However, these children outside the cohort did show a slightly higher prevalence and intensity of S. haematobium infection than those in the cohort as in Table 1 (P < 0.01) at 2 years post-treatment.
Fig. 2. Changes in the category of intensity of Schistosoma haematobium infection in schoolchildren: cross-sectional data 2 years post-treatment (n=761) compared with baseline data (n=1644)
Table 2. Cross-sectional analysis of Schistosoma haematobium infection in the 7–14-year-old schoolchildren before and after treatment
Comparison of 3-year data from the 7-year-old schoolchildren
Only S. haematobium infection is presented here, as the infection level for other helminths was low. As in Table 3 (available at: http://www.who.int/bulletin/volumes/86/10/07-048694/en/index.html), similar to the cohort data, 1 year after treatment overall both prevalence and intensity of S. haematobium infection in the 7-year-old children showed a dramatic reduction, by an average of 82.9% and 92.3% respectively (P < 0.01). There was a significant uptrend in both overall prevalence and intensity of infection 2 years post-treatment compared with 1 year post-treatment (P < 0.01), but the overall level of prevalence and intensity of infection was still far below the original level by 65.9% and 78.4% respectively (P < 0.01). More importantly, the proportion of heavy infections (≥ 50 e/10 ml) remained lower at 2.5% 2 years later compared with 14% before treatment (Fig. 3). The trend in different regions and in both genders was generally similar with prevalence and intensity of infection post-treatment being significantly lower than at baseline (P < 0.01) except in the south-west (Sud Ouest) region. There, the boys showed a significant increase in both prevalence and intensity of infection 2 years post-treatment compared to one year post-treatment, while girls did not.
Fig. 3. Changes in the category of intensity of Schistosoma haematobium infection in the 7-year-old first-year schoolchildren before treatment (n=154), 1 year post-treatment (n=307) and 2 years post-treatment (n=317)
Table 3. Cross-sectional analysis of Schistosoma haematobium infection in the 7-year-old first-year schoolchildren before and after treatmenta
S. mansoni infection
Longitudinal cohort data
Parasitological results on S. mansoni infection in the longitudinal cohort children successfully examined at baseline and followed-up one year and two years post-treatment are summarized in Table 4 (available at: http://www.who.int/bulletin/volumes/86/10/07-048694/en/index.html). S. mansoni infection was detected only in the Sud Ouest region in sentinel schools with prevalence of 13.6% and intensity of infection of 22.4 epg in the region. Two years after treatment these were significantly reduced to 1.5% and 2.9 epg respectively (P < 0.05).
Table 4. Schistosoma mansoni prevalence and intensity of infection in the longitudinal cohort children before and after treatmenta
In the cross-sectional data, S. mansoni infection was also shown only in the Sud Ouest region. In baseline children (7–14 years old) in the original cohort in this region, prevalence of S. mansoni infection was 14.2% (95% CI: 10.8–17.6; n = 408) and intensity of infection was 23.0 epg (95% CI: 11.8–34.2; n = 408) before treatment. Two years after treatment, S. mansoni prevalence in this region was 7.6% (95% CI: 4.4–11.0; n = 248) and intensity of infection was 16.5 epg (95% CI: 1.9–31.0; n = 248) (both P < 0.05).
In line with previous findings,12 S. haematobium infection was found prevalent throughout cohort schools in the country with very high levels of infection in the north, particularly in the Sahel region where infection was nearly universal in some schools (details not shown), and a moderate level of infection in the Sud Ouest region. Although S. haematobium infection was relatively low in the Sud Ouest compared with other regions, S. mansoni infection was also found to be prevalent. Therefore, the combined prevalence of schistosomiasis was actually very high, reaching nearly 50% in the longitudinal data and more than 30% in the cross-sectional data at baseline. The baseline data confirmed the significant burden caused by schistosomiasis to school-age children in Burkina Faso. We also found universally low STH infections (data not shown). This may be due to the fact that the national control programme on lymphatic filariasis using albendazole and ivermectin started in 2001, and several rounds of treatment had already been implemented in some areas of the country.19,20
Impact of treatment
A single treatment significantly reduced S. haematobium infection in the country and kept it low for the following 2 years. Two years after treatment, prevalence of S. haematobium infection in school-age children was still at a significantly lower level than at baseline and, more importantly, intensity of infection remained at a low level. The proportion of heavy infections was greatly reduced. This is particularly important as high intensity of S. haematobium infection has been shown to contribute to morbidity, including anaemia, in children.14 The reduction in prevalence and intensity of infection was confirmed by both longitudinal cohort follow-up and cross-sectional survey. In previous small-scale studies on S. haematobium control in eastern Africa, an annual treatment strategy was predominantly used, with varying results.21,22 However, in western Africa, one study in the Niger showed that, 3 years after a single PZQ treatment, prevalence and intensity of S. haematobium infection remained significantly lower than at baseline.23,24 In another study in Ghana, with one single PZQ treatment, intensity of S. haematobium infection was reduced by 80–99% 12 months after treatment and remained very low in two of three study areas 24 months after treatment.25 Our results are in line with these studies, suggesting that a more spaced treatment strategy, as implemented in Burkina Faso, is highly effective on S. haematobium infections, even in highly-endemic areas. In addition, we also observed a significant reduction in S. mansoni infection during the 2 years after treatment.
One of the factors likely to have contributed to the great impact demonstrated in Burkina Faso is the high nationwide treatment coverage (over 90%) achieved in a relatively short space of time by the control programme.11 Another factor is that 2004 was a very dry year and treatment was delivered in the dry season. These two important factors together may have helped to reduce transmission26 and, therefore, should be considered when implementing a national control programme in other sub-Saharan countries to maximize the treatment impact. Nevertheless, the general uptrend of the prevalence and intensity of S. haematobium infection shown 2 years post-treatment, compared with 1 year post-treatment, could also signal a potential rebound of S. haematobium infection should drug distribution be interrupted. This therefore highlights the importance of continued effort in monitoring disease transmission and of repeated treatment when and where necessary.
Throughout the 2 years, the drop-out rate of cohort children was high, particularly in the Sud Ouest region where very few original cohort children were traced and re-examined at both follow-ups. One of the main reasons for the loss of cohort children was family migration, which is very common in the country and particularly in this region (Seydou Touré, personal observation). Another of the main reasons was that a proportion of the original cohort (older age groups) had naturally progressed to secondary schools over the study period. High drop-out is indeed a relatively common problem in the monitoring activities of our programmes in sub-Saharan Africa.
Unlike in Uganda,9,10 a biennial treatment of school-age children (5–15 years old) through school-based and community-based drug deliveries was implemented in Burkina Faso. This decision was based on previous experience with S. haematobium in western Africa23–25 and on the fact that the ongoing monitoring and evaluation activities showed a low level of infection 1 year post-treatment.14 Current results, together with previous findings by others,23–25 suggest that the WHO-recommended treatment strategies on urinary schistosomiasis should be adopted with some degree of flexibility according to different epidemiological and geographical settings. Provided that coverage is high and is implemented in a dry season, treatment once every two years may be sufficient, even in highly-endemic regions such as Sahel and Boucle du Mouhoun, and in less endemic regions perhaps treatment every three or more years could equally prove sufficient. It is however more difficult to make inferences on the appropriate interval of treatment on intestinal schistosomiasis from the current data because of the relatively small number of individuals with such infection enrolled in our survey, and the lower levels of infection registered. Our study also suggests that monitoring and evaluation is a crucial component of the national control programme for fine-tuning a treatment strategy according to national and local epidemiological conditions.
Previous analysis has shown that in Burkina Faso, the total costs per child treated against schistosomiasis and STH, including drug and delivery, was US$ 0.32.11 A possible further reduction of treatment frequency for urinary schistosomiasis, where applicable, is expected to further reduce the overall costs of the control activities. The current national control programme in Burkina Faso has recently entered a new phase – integrated control of neglected tropical diseases.27,28 The next rounds of treatment are planned to be delivered in an integrated manner to include schistosomiasis, STH, lymphatic filariasis, onchocerciasis and trachoma.5 In this framework, the best way to tackle schistosomiasis is being assessed. Treatment with reduced frequency plus integrated control strategies may significantly increase the sustainability of national control programmes in Burkina Faso and in the rest of sub-Saharan Africa.
This study showed that a significant impact on urinary schistosomiasis was achieved by biennial distribution of PZQ with high coverage rates in Burkina Faso. We demonstrated, for the first time on a national scale, that such treatment frequency can be successfully applied to control urinary schistosomiasis in sub-Saharan Africa. This may provide a cost-effective treatment strategy for similar national schistosomiasis control programmes in resource-limited settings. ■
We thank all the staff at the Programme National de Lutte contre la Schistosomiase et les Vers Intestinaux, Ministère de la Santé, Burkina Faso, and Ruairidh Crawford for his data analysis during his student project.
Funding: The Schistosomiasis Control Initiative is sponsored by the Bill and Melinda Gates Foundation, which had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: None declared.
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- Programme National de Lutte contre la Schistosomiase et les Vers Intestinaux, Ministère de la Santé, Ouagadougou, Burkina Faso.
- Schistosomiasis Control Initiative, Imperial College London, Norfolk Place, London, W2 1PG, England.
- Department of Control of Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland.
- Réseau International Schistosomoses, Environnement, Aménagements et Lutte (RISEAL), Ploemeur, France.