Trans R Soc Trop Med Hyg doi:10.1093/trstmh/trv008
REVIEW
Are health education interventions effective for the control and prevention of urogenital schistosomiasis in sub-Saharan Africa? A systematic review Amy Pricea,*, Arpana Vermab and William Welfareb a
University of Manchester Medical School; bManchester Academic Health Sciences Centre, Institute of Population Health, Stopford Building, MAHSC, University of Manchester, Manchester, M13 9PT, UK *Corresponding author: Tel: +44 (0) 751 168 5047; E-mail: [email protected]
Received 17 November 2014; revised 30 December 2014; accepted 19 January 2015 An estimated 129 million people are infected with urogenital schistosomiasis in sub-Saharan Africa. Current control recommendations endorse mass administration of praziquantel. Health education is an important component of effective schistosomiasis prevention and control, but there has been limited research on its effectiveness. This paper reviews the effectiveness of health education as an intervention in the prevention and control of urogenital schistosomiasis in sub-Saharan Africa. The outcomes of interest were prevalence, incidence or transmission of schistosomiasis, behaviour change associated with infection, or changes in knowledge of the disease. The findings from this review suggest that health education has a beneficial impact on knowledge and understanding of schistosomiasis within the target groups. However, further research is needed due to the poor quality of the included studies. Keywords: Health education, Patient education, Schistosomiasis haematobium, Sub-Saharan Africa
Introduction Schistsosomiasis or bilharzia is a chronic parasitic disease caused by blood dwelling fluke worms of the genus Schistosoma. It is common in tropical and sub-tropical countries, especially in poor communities with little access to clean water and basic sanitation. There are three main species of Schistosoma that are known to infect humans. These include Schistosoma haematobium, S. japonicum and S. mansoni. Only S. haematobium causes urogenital schistosomiasis, as the remaining species cause intestinal schistosomiasis.1 Recent information from WHO shows that the geographical distribution of S. haematobium is limited to Africa and the Middle East.2 Worldwide, there are estimated to be 207 million people infected with Schistosoma spp.;3 93% of whom live in sub-Saharan Africa.4 Approximately 67% of the cases of schistosomiasis in sub-Saharan Africa are due to S. haematobium, rendering urogenital schistosomiasis a significant public health problem.5 The transmission of schistosomiasis requires contamination of surface water by urine of infected individuals, the presence of an intermediate snail host and humans coming into contact with freshwater.6 As the spread of the disease occurs through natural open freshwater, communities without access to safe water sources and with poor sanitation and hygiene are at a higher risk of infection.
Chronic infection with S. haematobium is known to have a significant impact on health. Studies have shown that long-term infection by the parasite can lead to haematuria, urinary stones,7 bladder cancer and renal failure.8 Schistosomiasis can cause female infertility9 and genital lesions that may increase the likelihood of HIV infection.10,11 In children the disease is associated with anaemia, reduced physical fitness12,13 and impaired cognitive development.14
Current treatment recommendations In 2001, the 54th World Health Assembly officially endorsed mass administration of anti-helminthic drugs as the key strategy for the treatment of schistosomiasis,15 and the Schistosomiasis Control Initiative (SCI) (Imperial College, London, UK) was created to help implement this.16 WHO guidelines recommend praziquantel as the drug of choice for the treatment of schistosomiasis, and recommend that it should be administered once every year in high-risk communities (prevalence .50%) and once every 2 years in moderate-risk communities (prevalence .20% and ,50%).17 Individuals eligible for mass drug administration include school-age children and adults considered to be at risk (including pregnant and lactating mothers, and those whose professions involve prolonged contact with potentially infected water).
# The Author 2015. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please e-mail: [email protected].
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Emerging concerns Praziquantel is effective in the treatment of schistosomiasis,18,19 but the global burden of schistosomiasis remains high.14 Multiple reasons could account for this, including failure of the mass drug administration programmes to effectively target all at-risk populations. According to the 2012 WHO report the proportion of patients in the African region treated for schistosomiasis was only 13.6% of the population estimated to require preventative chemotherapy.20 This low treatment rate is partially explained by a lack of global availability of praziqunatel, although recent donations from Merck KgaA, the United States Agency for International Development and the British Department for International Development have improved the situation.21 It is estimated that approximately 1200 million praziquantel tablets are required each year to treat all at-risk patients, at an annual cost of US$100 million, with an additional US$100 million required annually for distribution costs.22 The long-term effectiveness of mass drug administration has also been questioned: while it can reduce prevalence of the disease in the short term, it is not effective at eliminating the disease entirely.23 Poor sanitation and recurrent contact with infected water result in rapid re-infection following treatment.24 Treatment compliance among targeted populations has also shown to be hugely problematic. In one study conducted in Uganda in collaboration with the SCI, only 31% of those treated in 2004 were willing to be re-treated the following year, highlighting that patients are increasingly rejecting free treatment. Interviews with participants showed that many were concerned about the side effects of praziqauntel, fearing the drug would cause infertility, miscarriage and even death, with many also failing to understand the need for repeated doses of treatment when they do not have symptoms. The authors cite a lack of understanding about the disease and its treatment, as a result of inadequate health education, as a reason for the low rate of compliance.25 These obstacles highlight the need for strategies in addition to mass drug administration. One potential additional strategy is improving health education. Increased knowledge about schistosomiasis prevention and transmission might improve compliance with the preventative chemotherapy programme and reduce exposure to the parasite. The importance of health education in the control and treatment of schistosomiasis has been highlighted in a number of publications.26–29 This review aims to evaluate, in a systematic way, the existing literature pertaining to the effectiveness of health education interventions for the control of urogenital schistosomiasis in sub-Saharan Africa.
Materials and methods Our aim was to include studies that delivered health education interventions in a country in sub-Saharan Africa (as defined in reference30), published between 1980 and 2014, which included a comparative group (this may be either a control group, or may be a comparison between the same group pre- and post- intervention). Measured outcomes of the studies must examine the relationship between the health education intervention and either S. haematobium prevalence, incidence or transmission rates; changes in behaviour associated with infection; changes in knowledge of urogenital schistosomiasis.
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Box 1. Summary of inclusion criteria Population: Participants of any age and gender. Studies must be conducted in a country in sub-Saharan Africa (as defined in reference30). Intervention: Interventions must include some form of health education, conducted either in a community setting, a health facility or within schools. Study design: Randomised control trials, experimental and quasi-experimental studies. A comparative group must be included, this may be either a control group, or may be a comparison between the same group pre- and post-intervention. Outcomes: Must examine the relationship between the health education intervention and either S. haematobium prevalence, incidence or transmission rates; changes in behaviour associated with infection; changes in knowledge of urogenital schistosomiasis. Time range: 1980–2014
We searched Ovid Medline, Embase and CINAHL for relevant studies using the term: (Schistosomiasis haematobium) AND (Health education OR Patient education OR Health behaviour OR Health knowledge). Other search terms including ‘bilharzia,’ ‘urinary schistosomiasis,’ ‘intervention’ and ‘trial’ were also trialed but were not included in the final search, as they did not yield any additional articles. The search was conducted in February 2014. The reference lists were imported into RefWorks and duplicates were removed. One author (AP) selected the studies from the search results by first screening the titles, and then the abstracts to determine if they met the inclusion criteria for this review. If, according to the abstract screening, the papers were deemed to be compliant with the inclusion criteria, or if this could not be assessed from the abstract, then the full paper was read in order to determine whether it should be included in the final review. The characteristics of all studies included in the full paper screen including study design, participant demographics, measured outcomes, results, methodological limitations and reasons for inclusion or exclusion were extracted into a table summary. A second reviewer (author WW) then independently assessed all search criteria and excluded and included studies. A third reviewer (author AV) then acted as an arbitrator to settle any debates over which studies should be included or excluded. Box 1 is a summary of the inclusion criteria and Figure 1 shows a flow chart of the selected papers.
Results The initial database search identified 89 papers in total. Four additional papers were identified through hand searching. Removal of duplicates brought the total number to 81. The titles, abstracts and full text of these papers were then assessed to determine whether they complied with the inclusion criteria. Six papers were included in the final review.
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Figure 1. Flow chart of selected papers in this review.
Study characteristics 31–34
Four out of the six studies were quasi-experimental studies, one was a time series study35 and one was a randomised control trial.36 Five of the studies included a control group,31,33,34,36,37 and one compared the same group before and after intervention.35 The number of participants also varied widely between studies. Lucien et al.32 had the greatest number of participants with 1391, and Stothard et al.33 had the smallest number with 229 participants. Four studies solely used participants who were school children, with only two including participants over the age of 19.31,34
Interventions, measures and outcomes All six studies included some form of health education as an intervention. In two studies health education was delivered in combination with praziquantel treatment.31,34 In the remaining four studies, health education was the only intervention. The included studies delivered their health education interventions in a variety of settings, using a variety of methods. Cline et al.31 trained elementary school teachers and local health centres in five villages in Cameroon to deliver important educational messages to school children and village residents twice yearly (August–October and February–April) over a 2-year period (1991–1993). These health education messages were designed
to build on existing knowledge and practices, and emphasised reducing contamination of water sources. The study fails to describe the educational messages beyond this. This study delivered health education in combination with other interventions such as praziquantel treatment and snail control. The impact of these interventions was assessed both before and 2 years after implementation, and a control village was selected as a comparison for assessing the relative impact of the health education intervention. The main outcome used to assess health education was changes in knowledge about schistosomiasis, although the study does not specify how this was measured. The results of this study state that knowledge about the role of snails increased from 16 to 76%, and knowledge about water contact as the source of infection increased from 11% to 72% in the intervention village, compared to the control. Similarly, Garba et al.34 also intervened in both a classroom and a village setting in Niger. This study delivered health education messages to local villagers using discussion meetings run by the local health and sanitation clinic, and provided information to school children using a variety of health education materials including a film, five posters and two school information booklets. This health education programme was delivered for 5 years. At the end of this time period (February 1997), knowledge of schistosomiasis (including symptom recognition, disease transmission, control measures and changes in behaviour) was
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assessed using a questionnaire survey and the results from the five intervention villages were compared to the control village. The results show a statistically significant increase in knowledge of disease transmission and in the adoption of positive behaviour to reduce risk in the intervention villages compared to the control village. Lansdown et al.36 delivered a similar intervention in Tanzania in the form of a randomised control trial, with the difference that their teaching was only delivered to school children in a classroom setting. In this study, 50 schools in the Lushoto district were assigned to either a control or an intervention group. In the intervention group health education was delivered by Tanzanian school teachers following a 4-day training workshop for a duration of 5 months. The teaching methods used to deliver the health messages are not described in detail, but included interactive teaching methods such as songs, poetic dramas, visits and discussions and also daily health message boards displayed outside the classrooms. This was also the only study that used randomisation to select the control and intervention schools. The impact of the intervention was evaluated using a questionnaire to ascertain children’s health knowledge, focus groups and observations of changes in practice in schools. Measures were taken at baseline (March 1998), 9 months after the start of the health education intervention and as a follow-up enquiry 15 months after the end of the project. A statistically significant increase in knowledge of prevention of infection was seen in the intervention group, while no change was seen in the control group. Focus group discussions identified important barriers to health education. Suzuki et al.35 also intervened in a classroom setting, but the exact form of the intervention is not specified. The measures to assess the outcome however, are well described and involved administration of a knowledge, attitudes, belief and practices (KABP) survey three times in succession (at baseline, preexamination, and post-examination after 1 year). Correlation between the educational effect and infection rate was also assessed. Results showed that the mean score of the subject group increased by 13% (p¼0.001) in all genres. No clear correlation between infection rate and the educational effect was seen. Lucien et al.32 also measured the impact of delivering health education in classroom setting, but compared a pre-designed health education programme with one that was created by the school children themselves. A control group received no educational intervention. The exact format of these interventions is unclear. The outcome measures used in this study included prevalence of infection (measured via detection of haematuria and S. haematobium ova recovery from urine samples) and awareness of urogenital schistosomiasis (measured via a questionnaire survey) both pre- and 8-months post-intervention. Results show a significant increase in awareness of the disease in both intervention groups, but not in the control group. The increase was greater in the group where children were asked to design their own intervention. The results also show a strong negative correlation between the perception and prevalence of the disease in the two intervention groups. Stothard et al.33 delivered health education messages to school children through the structured use of a purpose-designed comic book over the course of 1 full school week. The impact of the booklet was measured by assessing and comparing knowledge and attitudes (KA) questionnaire scores both pre- and 1- week post-intervention. A positive increase in KA scores was
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found post- intervention, however these were not statistically significant. All six studies measured the impact of health education on knowledge and understanding of urogenital schistosomiasis. The results indicate that health education had a beneficial impact on knowledge and understanding of schistosomiasis within the target groups, although this was only found to be significant in five of the studies. Four of the studies included additional measures other than knowledge and awareness of the disease. Lucien et al.32 looked at the relationship between perception and prevalence of the disease, and found a negative correlation between these two variables, indicating that prevalence is inversely proportionate to awareness. Suzuki et al.35 looked at the relationship between infection rate and education effect, but no significant relationship was identified. Lansdown et al.36 and Garba et al.34 both used a survey to observe any health-related behaviour changes postintervention. The results from the follow-up survey used by Lansdown et al.36 show that 100% of intervention schools had improved sanitation and hygiene practices compared to only 63% of control schools. Garba et al.34 found that 33% of respondents in the intervention area reported adopting at least one positive behaviour to reduce risk compared with only 12% in the control area (p,0.001). These findings indicate that health education interventions can have a positive impact on health-related behaviour.
Discussion Overall, the review suggests that health education may be useful in the prevention of infection or re-infection with S. haematobium, as all six studies included in this review found that health education interventions increased knowledge and awareness of the disease. However, methodological limitations in almost all of the studies render the results subject to significant bias. Only two studies described the sampling methods used,34,36 and none of the six studies included a power calculation. Only one out of the six studies piloted their questionnaire33 and none validated it. Two of the studies did not describe the implemented health education interventions in detail,33,35 and failed to state both the teaching methods used and the length of time that the interventions were delivered for, making the results of these studies difficult to interpret or replicate. Those studies employing a health education intervention delivered by local teachers or community members seemed to have a greater impact. Their full involvement was achieved by means of planning, training workshops or focus groups. Neither Suzuki et al.35 or Stothard et al.33 employed these methods, and produced fairly modest results in comparison with those studies that did. Lucien et al.32 highlight this further as their study found that when a pre-designed intervention was compared with an intervention designed by the school children themselves, the latter had a much greater impact. However, a limited description of the methods used makes this finding difficult to fully understand and replicate. Although this review shows that health education interventions can increase disease knowledge and awareness, the subsequent impact it has on behaviour, infection and prevalence rates is difficult to assess.
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Suzuki et al.35 found no significant relationship between prevalence and the education effect. It is difficult to interpret this finding due to a lack of detail about their sampling methods, no apparent validation of the questionnaire or a power calculation. Lucien et al.32 found an inverse association between disease perception and prevalence. Once again lack of detail about the intervention makes these results difficult to interpret. Garba et al.34 surveyed the post- intervention knowledge and positive behaviour changes in the intervention villages and found a statistically significant increase in both of these compared to controls. However, the rates of participation in the educational programmes were low, as only 16% of survey respondents attended both a film screening and a discussion-based workshop, making it difficult to attribute these results solely to the intervention. Lansdown et al.36 measured behaviour changes post-intervention, and found that these were greater in the intervention schools compared to the control schools. This is probably the most reliable of the three studies as their sampling and intervention methods are well described, although a drop-out rate of 30% is of concern. Duration of the interventions is another important aspect to consider. This varied widely amongst the studies. Garba et al.34 had the longest intervention period of 5 years, whilst Stothard et al.38 had a much shorter intervention period of only 1 week. Stothard et al.38 was the only study that did not produce a statistically significant result with regards to the impact of health education on disease knowledge and awareness, and this may be attributable to the very short duration of the intervention. However, once again, due to a lack of detailed description of the intensity and duration of the educational interventions used in any of the studies the impact of this is difficult to fully assess and comprehend. Cost effectiveness is only discussed in two of the studies. Lansdown et al.36 delivered their health education programme at no cost to the schools themselves, and state that replication of this programme would only involve the costs of travel and board for the teachers during the initial training workshops. The educational programme delivered by Stothard et al.33 was more expensive as the cost of each booklet used was US$5. To fully understand the cost effectiveness of these interventions their long-term impact needs to be assessed and compared with the cost and sustainability of mass chemotherapy alone. This goes beyond the scope of this review.
perfect methodologies, most did not describe sampling methods and interventions, and the validity of outcome measures was not determined. Statistical analysis of the studies was also limited. All included studies did not account for baseline differences between the control and intervention groups. This review also has limitations: grey literature was not included in the search strategy, something that may have lead to bias in our results.
Conclusions The limitations of the mass chemotherapy approach highlight the need for additional interventions. WHO recognises the importance of such additional public health measures, and resolution WHA54.19 urges countries to encourage health education as a means of reducing disease transmission.15 Despite this there is limited research into health education in this context. This review aimed to review the effectiveness of health education in the prevention of urogenital schistosomiasis. These interventions appear to have a beneficial effect on knowledge and awareness of the disease in target populations. Further, well-designed research is urgently needed, as the evidence is limited. Studies included in this review highlight the importance of involving the community in the interventions as much as possible, and this is one area for further research.
Supplementary data Supplementary data are available at Transactions Online (http:// trstmh.oxfordjournals.org/).
Authors’ contributions: AP, AV and WW conceived the study; AP and AV designed the study protocol; AP carried out the literature search, and analysis and interpretation of the results; AP drafted the manuscript; AP, AV and WW critically revised the manuscript. All authors read and approved the final manuscript. AV is the guarantor of the paper. Funding: None. Competing interests: None declared.
Future research The poor methodology of the studies, combined with a poor description of the methods of teaching and the duration of the interventions show that further, well-designed research is essential. Overall, studies included in this review highlight the importance of involving the community in the interventions as much as possible, and future research should focus on discovering which teaching methods best achieve this. Some studies have also shown a possible link between health education and reduced disease prevalence, and this provides another important topic for future research.
Limitations Limitations of this review and of the individual studies must be acknowledged. Overall the included studies employed less than
Ethical approval: Not required.
References 1 Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006;368:1106–18. 2 WHO. Schistosomiasis - epidemiology. http://www.who.int/ schistosomiasis/epidemiology/table3/en/index.html [accessed 23 January 2014]. 3 Steinmann P, Keiser J, Bos R et al. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 2006;6:411–25. 4 Hotez PJ, Kamath A. Neglected tropical diseases in sub-saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis 2009;3:e412.
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5 van der Werf MJ, de Vlas SJ, Brooker S et al. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 2003;86:125–39. 6 CDC. Centre for Disease Control: Parasites- schistosomiasis 2012. http:// www.cdc.gov/parasites/schistosomiasis/biology.html [accessed 23 January 2014]. 7 Smith JH, Christie JD. The pathobiology of Schistosoma haematobium infection in humans. Hum Pathol 1986;17:333–45. 8 Rollinson D. A wake up call for urinary schistosomiasis: reconciling research effort with public health importance. Parasitology 2009;136:1593–610. 9 El-Mahgoub S. Pelvic schistosomiasis and infertility. Int J Gynecol Obstet 1982;20:201–6. 10 Poggensee G, Feldmeier H. Female genital schistosomiasis: facts and hypotheses. Acta Trop 2001;79:193–210. 11 Kjetland EF, Ndhlovu PD, Gomo E et al. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 2006;20:593–600. 12 Stephenson LS, Latham MC, Kurz KM et al. Urinary iron loss and physical fitness of Kenyan children with urinary schistosomiasis. Am J Trop Med Hyg 1985;34:322–30. 13 Prual A, Daouda H, Develoux M et al. Consequences of Schistosoma haematobium infection on the iron status of schoolchildren in Niger. Am J Trop Med Hyg 1992;47:291–7. 14 King CH, Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chronic Illn 2008;4:65–79. 15 WHO Expert Committee. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 2002;912:1–57. 16 Stothard JR, Chitsulo L, Kristensen TK, Utzinger J. Control of schistosomiasis in sub-Saharan Africa: Progress made, new opportunities and remaining challenges. Parasitology 2009;136:1665–75. 17 WHO. Preventive chemotherapy in human helminthiasis. Coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: World Health Organization; 2006. 18 Toure S, Zhang Y, Bosque-Oliva E et al. Two-year impact of single praziquantel treatment on infection in the national control programme on schistosomiasis in Burkina Faso. Bull World Health Organ 2008;86:780–7. 19 French MD, Churcher TS, Gambhir M et al. Observed reductions in Schistosoma mansoni transmission from large-scale administration of praziquantel in Uganda: a mathematical modelling study. PLoS Negl Trop Dis 2010;4:e897. 20 WHO. Schistosomiasis: number of people receiving preventive chemotherapy in 2012. Wkly Epidemiol Rec 2014;89:21–8. 21 WHO. Schistosomiasis: progress report 2001–2011, strategic plan 2012–2020. Geneva: World Health Organization; 2013.
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22 Hotez PJ, Fenwick A. Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Negl Trop Dis 2009;3:e485. 23 Satayathum SA, Muchiri EM, Ouma JH et al. Factors affecting infection or reinfection with Schistosoma haematobium in coastal Kenya: survival analysis during a nine-year, school-based treatment program. Am J Trop Med Hyg 2006;75:83–92. 24 Freudenthal S, Ahlberg BM, Mtweve S et al. School-based prevention of schistosomiasis: initiating a participatory action research project in northern Tanzania. Acta Trop 2006;100:79–87. 25 Parker M, Allen T, Hastings J. Resisting control of neglected tropical diseases: dilemmas in the mass treatment of schistosomiasis and soil-transmitted helminths in north-west Uganda. J Biosoc Sci 2008;40:161–81. 26 Asaolu SO, Ofoezie IE. The role of health education and sanitation in the control of helminth infections. Acta Trop 2003;86:283–94. 27 Utzinger J, Raso G, Brooker S et al. Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology 2009;136:1859–74. 28 Wang L, Guo J, Wu X et al. China’s new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Trop Med Int Health 2009;14:1475–83. 29 Garba A, Toure´ S, Dembele´ R et al. Implementation of national schistosomiasis control programmes in West Africa. Trends Parasitol 2006;22:322–6. 30 Library of Congress. List of Sub-Saharan African Countries. http://www. loc.gov/rr/amed/guide/afr-countrylist.html [accessed 23 January 2014]. 31 Cline BL, Hewlett BS. Community-based approach to schistosomiasis control. Acta Trop 1996;61:107–19. 32 Lucien KF, Nkwelang G, Ejezie GC. Health education strategy in the control of urinary schistosomiasis. Clin Lab Sci 2003;16:137–41. 33 Stothard JR, Mook P, Mgeni AF et al. Control of urinary schistosomiasis on Zanzibar (Unguja Island): a pilot evaluation of the educational impact of the Juma na Kichocho health booklet within primary schools. Mem Inst Oswaldo Cruz 2006;101 (Suppl 1):119–24. 34 Garba A, Aboubacar A, Barkire A et al. Impact of health education progams on the control of urinary bilharziasis in Niger [in French]. Sante´ 2001;11:35–42. 35 Suzuki C, Mizota T, Awazawa T et al. Effects of a school-based education program for schistosomiasis control. Southeast Asian J Trop Med Public Health 2005;36:1388–93. 36 Lansdown R, Ledward A, Hall A et al. Schistosomiasis, helminth infection and health education in Tanzania: achieving behaviour change in primary schools. Health Educ Res 2002;17:425–33. 37 Lucien KF, Nkwelang G, Ejezie GC. Health education strategy in the control of urinary schistosomiasis. Clin Lab Sci 2003;16:137–41. 38 Stothard JR, Mook P, Mgeni AF. Control of urinary schistosomiasis on Zanzibar (Unguja Island): a pilot evaluation of the educational impact of the Juma na Kichocho health booklet within primary schools. Mem Inst Oswaldo Cruz 2006 Sep;101 (Suppl 1):119–24.
REVIEW
Are health education interventions effective for the control and prevention of urogenital schistosomiasis in sub-Saharan Africa? A systematic review Amy Pricea,*, Arpana Vermab and William Welfareb a
University of Manchester Medical School; bManchester Academic Health Sciences Centre, Institute of Population Health, Stopford Building, MAHSC, University of Manchester, Manchester, M13 9PT, UK *Corresponding author: Tel: +44 (0) 751 168 5047; E-mail: [email protected]
Received 17 November 2014; revised 30 December 2014; accepted 19 January 2015 An estimated 129 million people are infected with urogenital schistosomiasis in sub-Saharan Africa. Current control recommendations endorse mass administration of praziquantel. Health education is an important component of effective schistosomiasis prevention and control, but there has been limited research on its effectiveness. This paper reviews the effectiveness of health education as an intervention in the prevention and control of urogenital schistosomiasis in sub-Saharan Africa. The outcomes of interest were prevalence, incidence or transmission of schistosomiasis, behaviour change associated with infection, or changes in knowledge of the disease. The findings from this review suggest that health education has a beneficial impact on knowledge and understanding of schistosomiasis within the target groups. However, further research is needed due to the poor quality of the included studies. Keywords: Health education, Patient education, Schistosomiasis haematobium, Sub-Saharan Africa
Introduction Schistsosomiasis or bilharzia is a chronic parasitic disease caused by blood dwelling fluke worms of the genus Schistosoma. It is common in tropical and sub-tropical countries, especially in poor communities with little access to clean water and basic sanitation. There are three main species of Schistosoma that are known to infect humans. These include Schistosoma haematobium, S. japonicum and S. mansoni. Only S. haematobium causes urogenital schistosomiasis, as the remaining species cause intestinal schistosomiasis.1 Recent information from WHO shows that the geographical distribution of S. haematobium is limited to Africa and the Middle East.2 Worldwide, there are estimated to be 207 million people infected with Schistosoma spp.;3 93% of whom live in sub-Saharan Africa.4 Approximately 67% of the cases of schistosomiasis in sub-Saharan Africa are due to S. haematobium, rendering urogenital schistosomiasis a significant public health problem.5 The transmission of schistosomiasis requires contamination of surface water by urine of infected individuals, the presence of an intermediate snail host and humans coming into contact with freshwater.6 As the spread of the disease occurs through natural open freshwater, communities without access to safe water sources and with poor sanitation and hygiene are at a higher risk of infection.
Chronic infection with S. haematobium is known to have a significant impact on health. Studies have shown that long-term infection by the parasite can lead to haematuria, urinary stones,7 bladder cancer and renal failure.8 Schistosomiasis can cause female infertility9 and genital lesions that may increase the likelihood of HIV infection.10,11 In children the disease is associated with anaemia, reduced physical fitness12,13 and impaired cognitive development.14
Current treatment recommendations In 2001, the 54th World Health Assembly officially endorsed mass administration of anti-helminthic drugs as the key strategy for the treatment of schistosomiasis,15 and the Schistosomiasis Control Initiative (SCI) (Imperial College, London, UK) was created to help implement this.16 WHO guidelines recommend praziquantel as the drug of choice for the treatment of schistosomiasis, and recommend that it should be administered once every year in high-risk communities (prevalence .50%) and once every 2 years in moderate-risk communities (prevalence .20% and ,50%).17 Individuals eligible for mass drug administration include school-age children and adults considered to be at risk (including pregnant and lactating mothers, and those whose professions involve prolonged contact with potentially infected water).
# The Author 2015. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please e-mail: [email protected].
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Emerging concerns Praziquantel is effective in the treatment of schistosomiasis,18,19 but the global burden of schistosomiasis remains high.14 Multiple reasons could account for this, including failure of the mass drug administration programmes to effectively target all at-risk populations. According to the 2012 WHO report the proportion of patients in the African region treated for schistosomiasis was only 13.6% of the population estimated to require preventative chemotherapy.20 This low treatment rate is partially explained by a lack of global availability of praziqunatel, although recent donations from Merck KgaA, the United States Agency for International Development and the British Department for International Development have improved the situation.21 It is estimated that approximately 1200 million praziquantel tablets are required each year to treat all at-risk patients, at an annual cost of US$100 million, with an additional US$100 million required annually for distribution costs.22 The long-term effectiveness of mass drug administration has also been questioned: while it can reduce prevalence of the disease in the short term, it is not effective at eliminating the disease entirely.23 Poor sanitation and recurrent contact with infected water result in rapid re-infection following treatment.24 Treatment compliance among targeted populations has also shown to be hugely problematic. In one study conducted in Uganda in collaboration with the SCI, only 31% of those treated in 2004 were willing to be re-treated the following year, highlighting that patients are increasingly rejecting free treatment. Interviews with participants showed that many were concerned about the side effects of praziqauntel, fearing the drug would cause infertility, miscarriage and even death, with many also failing to understand the need for repeated doses of treatment when they do not have symptoms. The authors cite a lack of understanding about the disease and its treatment, as a result of inadequate health education, as a reason for the low rate of compliance.25 These obstacles highlight the need for strategies in addition to mass drug administration. One potential additional strategy is improving health education. Increased knowledge about schistosomiasis prevention and transmission might improve compliance with the preventative chemotherapy programme and reduce exposure to the parasite. The importance of health education in the control and treatment of schistosomiasis has been highlighted in a number of publications.26–29 This review aims to evaluate, in a systematic way, the existing literature pertaining to the effectiveness of health education interventions for the control of urogenital schistosomiasis in sub-Saharan Africa.
Materials and methods Our aim was to include studies that delivered health education interventions in a country in sub-Saharan Africa (as defined in reference30), published between 1980 and 2014, which included a comparative group (this may be either a control group, or may be a comparison between the same group pre- and post- intervention). Measured outcomes of the studies must examine the relationship between the health education intervention and either S. haematobium prevalence, incidence or transmission rates; changes in behaviour associated with infection; changes in knowledge of urogenital schistosomiasis.
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Box 1. Summary of inclusion criteria Population: Participants of any age and gender. Studies must be conducted in a country in sub-Saharan Africa (as defined in reference30). Intervention: Interventions must include some form of health education, conducted either in a community setting, a health facility or within schools. Study design: Randomised control trials, experimental and quasi-experimental studies. A comparative group must be included, this may be either a control group, or may be a comparison between the same group pre- and post-intervention. Outcomes: Must examine the relationship between the health education intervention and either S. haematobium prevalence, incidence or transmission rates; changes in behaviour associated with infection; changes in knowledge of urogenital schistosomiasis. Time range: 1980–2014
We searched Ovid Medline, Embase and CINAHL for relevant studies using the term: (Schistosomiasis haematobium) AND (Health education OR Patient education OR Health behaviour OR Health knowledge). Other search terms including ‘bilharzia,’ ‘urinary schistosomiasis,’ ‘intervention’ and ‘trial’ were also trialed but were not included in the final search, as they did not yield any additional articles. The search was conducted in February 2014. The reference lists were imported into RefWorks and duplicates were removed. One author (AP) selected the studies from the search results by first screening the titles, and then the abstracts to determine if they met the inclusion criteria for this review. If, according to the abstract screening, the papers were deemed to be compliant with the inclusion criteria, or if this could not be assessed from the abstract, then the full paper was read in order to determine whether it should be included in the final review. The characteristics of all studies included in the full paper screen including study design, participant demographics, measured outcomes, results, methodological limitations and reasons for inclusion or exclusion were extracted into a table summary. A second reviewer (author WW) then independently assessed all search criteria and excluded and included studies. A third reviewer (author AV) then acted as an arbitrator to settle any debates over which studies should be included or excluded. Box 1 is a summary of the inclusion criteria and Figure 1 shows a flow chart of the selected papers.
Results The initial database search identified 89 papers in total. Four additional papers were identified through hand searching. Removal of duplicates brought the total number to 81. The titles, abstracts and full text of these papers were then assessed to determine whether they complied with the inclusion criteria. Six papers were included in the final review.
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Figure 1. Flow chart of selected papers in this review.
Study characteristics 31–34
Four out of the six studies were quasi-experimental studies, one was a time series study35 and one was a randomised control trial.36 Five of the studies included a control group,31,33,34,36,37 and one compared the same group before and after intervention.35 The number of participants also varied widely between studies. Lucien et al.32 had the greatest number of participants with 1391, and Stothard et al.33 had the smallest number with 229 participants. Four studies solely used participants who were school children, with only two including participants over the age of 19.31,34
Interventions, measures and outcomes All six studies included some form of health education as an intervention. In two studies health education was delivered in combination with praziquantel treatment.31,34 In the remaining four studies, health education was the only intervention. The included studies delivered their health education interventions in a variety of settings, using a variety of methods. Cline et al.31 trained elementary school teachers and local health centres in five villages in Cameroon to deliver important educational messages to school children and village residents twice yearly (August–October and February–April) over a 2-year period (1991–1993). These health education messages were designed
to build on existing knowledge and practices, and emphasised reducing contamination of water sources. The study fails to describe the educational messages beyond this. This study delivered health education in combination with other interventions such as praziquantel treatment and snail control. The impact of these interventions was assessed both before and 2 years after implementation, and a control village was selected as a comparison for assessing the relative impact of the health education intervention. The main outcome used to assess health education was changes in knowledge about schistosomiasis, although the study does not specify how this was measured. The results of this study state that knowledge about the role of snails increased from 16 to 76%, and knowledge about water contact as the source of infection increased from 11% to 72% in the intervention village, compared to the control. Similarly, Garba et al.34 also intervened in both a classroom and a village setting in Niger. This study delivered health education messages to local villagers using discussion meetings run by the local health and sanitation clinic, and provided information to school children using a variety of health education materials including a film, five posters and two school information booklets. This health education programme was delivered for 5 years. At the end of this time period (February 1997), knowledge of schistosomiasis (including symptom recognition, disease transmission, control measures and changes in behaviour) was
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assessed using a questionnaire survey and the results from the five intervention villages were compared to the control village. The results show a statistically significant increase in knowledge of disease transmission and in the adoption of positive behaviour to reduce risk in the intervention villages compared to the control village. Lansdown et al.36 delivered a similar intervention in Tanzania in the form of a randomised control trial, with the difference that their teaching was only delivered to school children in a classroom setting. In this study, 50 schools in the Lushoto district were assigned to either a control or an intervention group. In the intervention group health education was delivered by Tanzanian school teachers following a 4-day training workshop for a duration of 5 months. The teaching methods used to deliver the health messages are not described in detail, but included interactive teaching methods such as songs, poetic dramas, visits and discussions and also daily health message boards displayed outside the classrooms. This was also the only study that used randomisation to select the control and intervention schools. The impact of the intervention was evaluated using a questionnaire to ascertain children’s health knowledge, focus groups and observations of changes in practice in schools. Measures were taken at baseline (March 1998), 9 months after the start of the health education intervention and as a follow-up enquiry 15 months after the end of the project. A statistically significant increase in knowledge of prevention of infection was seen in the intervention group, while no change was seen in the control group. Focus group discussions identified important barriers to health education. Suzuki et al.35 also intervened in a classroom setting, but the exact form of the intervention is not specified. The measures to assess the outcome however, are well described and involved administration of a knowledge, attitudes, belief and practices (KABP) survey three times in succession (at baseline, preexamination, and post-examination after 1 year). Correlation between the educational effect and infection rate was also assessed. Results showed that the mean score of the subject group increased by 13% (p¼0.001) in all genres. No clear correlation between infection rate and the educational effect was seen. Lucien et al.32 also measured the impact of delivering health education in classroom setting, but compared a pre-designed health education programme with one that was created by the school children themselves. A control group received no educational intervention. The exact format of these interventions is unclear. The outcome measures used in this study included prevalence of infection (measured via detection of haematuria and S. haematobium ova recovery from urine samples) and awareness of urogenital schistosomiasis (measured via a questionnaire survey) both pre- and 8-months post-intervention. Results show a significant increase in awareness of the disease in both intervention groups, but not in the control group. The increase was greater in the group where children were asked to design their own intervention. The results also show a strong negative correlation between the perception and prevalence of the disease in the two intervention groups. Stothard et al.33 delivered health education messages to school children through the structured use of a purpose-designed comic book over the course of 1 full school week. The impact of the booklet was measured by assessing and comparing knowledge and attitudes (KA) questionnaire scores both pre- and 1- week post-intervention. A positive increase in KA scores was
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found post- intervention, however these were not statistically significant. All six studies measured the impact of health education on knowledge and understanding of urogenital schistosomiasis. The results indicate that health education had a beneficial impact on knowledge and understanding of schistosomiasis within the target groups, although this was only found to be significant in five of the studies. Four of the studies included additional measures other than knowledge and awareness of the disease. Lucien et al.32 looked at the relationship between perception and prevalence of the disease, and found a negative correlation between these two variables, indicating that prevalence is inversely proportionate to awareness. Suzuki et al.35 looked at the relationship between infection rate and education effect, but no significant relationship was identified. Lansdown et al.36 and Garba et al.34 both used a survey to observe any health-related behaviour changes postintervention. The results from the follow-up survey used by Lansdown et al.36 show that 100% of intervention schools had improved sanitation and hygiene practices compared to only 63% of control schools. Garba et al.34 found that 33% of respondents in the intervention area reported adopting at least one positive behaviour to reduce risk compared with only 12% in the control area (p,0.001). These findings indicate that health education interventions can have a positive impact on health-related behaviour.
Discussion Overall, the review suggests that health education may be useful in the prevention of infection or re-infection with S. haematobium, as all six studies included in this review found that health education interventions increased knowledge and awareness of the disease. However, methodological limitations in almost all of the studies render the results subject to significant bias. Only two studies described the sampling methods used,34,36 and none of the six studies included a power calculation. Only one out of the six studies piloted their questionnaire33 and none validated it. Two of the studies did not describe the implemented health education interventions in detail,33,35 and failed to state both the teaching methods used and the length of time that the interventions were delivered for, making the results of these studies difficult to interpret or replicate. Those studies employing a health education intervention delivered by local teachers or community members seemed to have a greater impact. Their full involvement was achieved by means of planning, training workshops or focus groups. Neither Suzuki et al.35 or Stothard et al.33 employed these methods, and produced fairly modest results in comparison with those studies that did. Lucien et al.32 highlight this further as their study found that when a pre-designed intervention was compared with an intervention designed by the school children themselves, the latter had a much greater impact. However, a limited description of the methods used makes this finding difficult to fully understand and replicate. Although this review shows that health education interventions can increase disease knowledge and awareness, the subsequent impact it has on behaviour, infection and prevalence rates is difficult to assess.
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Suzuki et al.35 found no significant relationship between prevalence and the education effect. It is difficult to interpret this finding due to a lack of detail about their sampling methods, no apparent validation of the questionnaire or a power calculation. Lucien et al.32 found an inverse association between disease perception and prevalence. Once again lack of detail about the intervention makes these results difficult to interpret. Garba et al.34 surveyed the post- intervention knowledge and positive behaviour changes in the intervention villages and found a statistically significant increase in both of these compared to controls. However, the rates of participation in the educational programmes were low, as only 16% of survey respondents attended both a film screening and a discussion-based workshop, making it difficult to attribute these results solely to the intervention. Lansdown et al.36 measured behaviour changes post-intervention, and found that these were greater in the intervention schools compared to the control schools. This is probably the most reliable of the three studies as their sampling and intervention methods are well described, although a drop-out rate of 30% is of concern. Duration of the interventions is another important aspect to consider. This varied widely amongst the studies. Garba et al.34 had the longest intervention period of 5 years, whilst Stothard et al.38 had a much shorter intervention period of only 1 week. Stothard et al.38 was the only study that did not produce a statistically significant result with regards to the impact of health education on disease knowledge and awareness, and this may be attributable to the very short duration of the intervention. However, once again, due to a lack of detailed description of the intensity and duration of the educational interventions used in any of the studies the impact of this is difficult to fully assess and comprehend. Cost effectiveness is only discussed in two of the studies. Lansdown et al.36 delivered their health education programme at no cost to the schools themselves, and state that replication of this programme would only involve the costs of travel and board for the teachers during the initial training workshops. The educational programme delivered by Stothard et al.33 was more expensive as the cost of each booklet used was US$5. To fully understand the cost effectiveness of these interventions their long-term impact needs to be assessed and compared with the cost and sustainability of mass chemotherapy alone. This goes beyond the scope of this review.
perfect methodologies, most did not describe sampling methods and interventions, and the validity of outcome measures was not determined. Statistical analysis of the studies was also limited. All included studies did not account for baseline differences between the control and intervention groups. This review also has limitations: grey literature was not included in the search strategy, something that may have lead to bias in our results.
Conclusions The limitations of the mass chemotherapy approach highlight the need for additional interventions. WHO recognises the importance of such additional public health measures, and resolution WHA54.19 urges countries to encourage health education as a means of reducing disease transmission.15 Despite this there is limited research into health education in this context. This review aimed to review the effectiveness of health education in the prevention of urogenital schistosomiasis. These interventions appear to have a beneficial effect on knowledge and awareness of the disease in target populations. Further, well-designed research is urgently needed, as the evidence is limited. Studies included in this review highlight the importance of involving the community in the interventions as much as possible, and this is one area for further research.
Supplementary data Supplementary data are available at Transactions Online (http:// trstmh.oxfordjournals.org/).
Authors’ contributions: AP, AV and WW conceived the study; AP and AV designed the study protocol; AP carried out the literature search, and analysis and interpretation of the results; AP drafted the manuscript; AP, AV and WW critically revised the manuscript. All authors read and approved the final manuscript. AV is the guarantor of the paper. Funding: None. Competing interests: None declared.
Future research The poor methodology of the studies, combined with a poor description of the methods of teaching and the duration of the interventions show that further, well-designed research is essential. Overall, studies included in this review highlight the importance of involving the community in the interventions as much as possible, and future research should focus on discovering which teaching methods best achieve this. Some studies have also shown a possible link between health education and reduced disease prevalence, and this provides another important topic for future research.
Limitations Limitations of this review and of the individual studies must be acknowledged. Overall the included studies employed less than
Ethical approval: Not required.
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