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      The Menace of Schistosomiasis in Nigeria: Knowledge, Attitude, and Practices Regarding Schistosomiasis among Rural Communities in Kano State

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          Abstract

          Background

          Schistosomiasis is one of the most common neglected tropical diseases, especially in the developing countries in Africa, Asia and South America, with Nigeria having the greatest number of cases of schistosomiasis worldwide. This community-based study aims to evaluate the knowledge, attitude and practices (KAP) regarding schistosomiasis among rural Hausa communities in Kano State, Nigeria.

          Methods

          A cross-sectional study was carried out among 551 participants from Hausa communities in five local government areas in Kano State, North Central Nigeria. Demographic, socioeconomic and environmental information as well as KAP data were collected using a pre-tested questionnaire. Moreover, faecal and urine samples were collected and examined for the presence of Schistosoma mansoni and S. haematobium eggs respectively.

          Results

          The overall prevalence of schistosomiasis was 17.8%, with 8.9% and 8.3% infected with S. mansoni and S. haematobium respectively, and 0.5% had co-infection of both species. Moreover, 74.5% of the participants had prior knowledge about schistosomiasis with 67.0% of them how it is transmitted and 63.8% having no idea about the preventive measures. Three-quarters of the respondents considered schistosomiasis a serious disease while their practices to prevent infections were still inadequate, with only 34.7% of them seeking treatment from clinics/hospitals. Significant associations between the KAP and age, gender, education and employment status were reported. Multiple logistic regression analysis revealed that age, gender, history of infection and educational level of the respondents were the most important factors significantly associated with the KAP on schistosomiasis among this population.

          Conclusions

          Schistosomiasis is still prevalent among Hausa communities in Nigeria and participants’ knowledge about the disease was poor. Mass drug administration, community mobilization and health education regarding the cause, transmission and prevention of schistosomiasis and education about good personal and sanitary hygiene practices should be considered in order to significantly reduce the prevalence and morbidity of infection within these communities.

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          Most cited references30

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          Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk.

          An estimated 779 million people are at risk of schistosomiasis, of whom 106 million (13.6%) live in irrigation schemes or in close proximity to large dam reservoirs. We identified 58 studies that examined the relation between water resources development projects and schistosomiasis, primarily in African settings. We present a systematic literature review and meta-analysis with the following objectives: (1) to update at-risk populations of schistosomiasis and number of people infected in endemic countries, and (2) to quantify the risk of water resources development and management on schistosomiasis. Using 35 datasets from 24 African studies, our meta-analysis showed pooled random risk ratios of 2.4 and 2.6 for urinary and intestinal schistosomiasis, respectively, among people living adjacent to dam reservoirs. The risk ratio estimate for studies evaluating the effect of irrigation on urinary schistosomiasis was in the range 0.02-7.3 (summary estimate 1.1) and that on intestinal schistosomiasis in the range 0.49-23.0 (summary estimate 4.7). Geographic stratification showed important spatial differences, idiosyncratic to the type of water resources development. We conclude that the development and management of water resources is an important risk factor for schistosomiasis, and hence strategies to mitigate negative effects should become integral parts in the planning, implementation, and operation of future water projects.
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            The role of health education and sanitation in the control of helminth infections.

            Health education and sanitation are two important components of primary health care system introduced by the World Health Organization (WHO) as a basis for the prevention and control of communicable diseases. However, the roles of health education and sanitation in disease control have been controversial, especially in the wake of recent advances in safe and effective oral drugs. This article has reviewed the various health education and sanitation interventions around the world to determine what roles they have played in the past relative to other intervention strategies and the role they have to play in future control efforts. It appears clear-cut from the review, that while chemotherapy has been and will remain the best option for morbidity control, sanitation has an important role to play not only to sustain the benefits of chemotherapy but also to protect the uninfected. Health education that is effective, simple and low-cost remains the only tool for creating the enabling environment for both chemotherapy and sanitation to thrive.
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              Parasitic Worms: Knowledge, Attitudes, and Practices in Western Côte d’Ivoire with Implications for Integrated Control

              Introduction Parasitic worms (helminths), such as soil-transmitted helminths and schistosomes, were so common in the 1940s that Norman W. Stoll coined the term “this wormy world” [1]. Helminths continue to affect hundreds of millions of people today. Indeed, more than half of the human population is at risk of soil-transmitted helminthiasis and schistosomiasis with more than 1 billion people infected, possibly causing a global burden of more than 40 million disability-adjusted life years (DALYs) lost annually [2]–[7]. Improvements have been made to reduce helminth transmission in many parts of the world [8], but worm infections continue to be an issue of major public health and socio-economic concern. Helmintic diseases disproportionately affect those in poverty [9], [10], with the poorest of the poor commonly suffering from multiple species infections concurrently [11]–[13]. In 2001 a resolution was passed during the 54th World Health Assembly (WHA) with the target (for member states) to regularly administer anthelmintic drugs to at least 75% and up to 100% of all school-aged children at risk of morbidity due to schistosomiasis and soil-transmitted helminthiasis by 2010 [14]. In the same year, the World Health Organization (WHO) assembled an expert committee to refine the global strategy for the prevention and control of schistosomiasis and soil-transmitted helminthiasis. Since then, millions of school-aged children have received anthelmintic drugs (albendazole or mebendazole against soil-transmitted helminthiasis and praziquantel against schistosomiasis) [15]–[17]. Comparatively little emphasis has been put on improving access to clean water and adequate sanitation and changing hygiene behavior, although these interventions represent an effective way for preventing intestinal parasitic infections, and are key factors for sustainable control [17]–[20]. Health education and promotion campaigns are essential for any change in behavior to be made. For health education and promotion activities to be effective, target audiences must be identified so that a clear message can be delivered, and hence local knowledge and perceptions must be taken into account [21]. Recent studies support that both individual and community perceptions and attitudes of parasitic worm infections and their prevention and treatment are important factors [22]–[24]. Over the past 15 years, we carried out research and control activities against schistosomiasis, soil-transmitted helminthiasis, and malaria in the region of Man in western Côte d'Ivoire, including studies which assessed local perceptions toward parasitic worm infection, drug intervention studies, risk mapping and prediction, and community-based control activities [25]–[32]. Here we describe knowledge, attitudes, practices (KAP) and behavior related to helminth infections in two rural communities of western Côte d'Ivoire that were subjected to either school-based or community-based research and control activities. The experience gained from this study might be useful for the design and implementation of an integrated control program and the lessons learned might stimulate other control programs to think and act beyond preventive chemotherapy. Methods Study area and historical context The Man region in western Côte d'Ivoire is populated by four main ethnic groups: Guéré, Toura, Wobé, and Yacouba. This study was conducted in the villages of Mélapleu (primarily Yacouba) and Zouatta II (primarily Wobé) between October 2003 and June 2004. Details of the study villages, with particular emphasis on intestinal helminth infections, have been described elsewhere [11], [25], [33]. At the time of the survey there were no health facilities available in either village. The health center nearest to Mélapleu was situated in the neighboring village of Gbatongouin, some 5 km east. With regard to Zouatta II, the nearest health center was located in Facobly, approximately 10 km away. In the district town of Man, some 25 km away from each village, there is a hospital. Of note, due to an armed conflict and socio-political unrest that occurred in Côte d'Ivoire since September 2002 [30], only the hospital of Man was functional at the time of the study and was run by the non-governmental organization ‘Médecins sans Frontiers’, providing free medical care for those in need. Apart the research activities undertaken by the Centre Suisse de Recherches Scientifiques en Côte d'Ivoire (CSRS), in partnership with the Université de Cocody-Abidjan and the Swiss Tropical and Public Health Institute (Swiss TPH), only very limited actions against schistosomiasis, soil-transmitted helminthiasis and malaria had taken place in this area. A pilot study was carried out in Mélapleu and two neighboring villages in 1996 to develop a questionnaire for the rapid identification of school children at risk of intestinal schistosomiasis [25]. Self-reported blood in stool proved a promising symptom, and hence the questionnaire was administered at the regional level, first in 1997 and again in 2002. Questionnaire results were validated with parasitological results obtained from 57–60 randomly selected schools using Kato-Katz thick smear examinations of stool samples from up to 100 children per school [26], [28]. The parasitological data were subsequently used for mapping and predicting the distribution of Schistosoma mansoni, hookworm, and S. mansoni-hookworm co-infections [29], [34]–[37]. In addition, a study was carried out in school children to assess the day-to-day and intra-specimen variation of S. mansoni egg output before and after praziquantel administration [34]. In Zouatta II, a multidisciplinary community-based study was implemented in 2002, consisting of a KAP survey pertaining to hygienic habits, water-contact and health-seeking behavior and in-depth appraisal of S. mansoni, soil-transmitted helminths, intestinal protozoa, and Plasmodium infections and multiparasitism among all family members living in 75 randomly selected households (more than half of the village) [11], [33], [38]. Infected individuals were treated and awareness was raised about how to prevent parasitic worm infections in the future with a small, local public health campaign at the time of the study. To better understand the perception and practices of parasitic worms, we used a combination of qualitative and quantitative methods. Data were then triangulated to verify and complete information gathered from communities. While the quantitative approach permitted us to obtain information on the frequency of people reporting signs and symptoms, causes, treatment and prevention of helmintic diseases, the qualitative data allowed us to further deepen the meaning of the diseases and to assess actual practice. Qualitative methods For the current study, a two-step qualitative approach was adopted. First, observations were made over a 2-week period at community places such as churches, local markets, schools, and water collection and washing sites. This enabled us to identify potential key informants and water contact sites for the second phase of the study. In addition, we observed and collected information on means of communication between formal and informal groups – such as youth, women, congregations, community assistance groups, and community leaders (e.g. meetings within and between groups, radio, and television). Finally, 30 focus group discussions (FGDs) and five semi-structured interviews were conducted. The FGDs (20 in Zouatta II, 10 in Mélapleu) were conducted with elderly women, adult women, adult men and school children. Common diseases, knowledge of signs and symptoms, causes, treatment, and prevention of schistosomiasis and intestinal helminths, as well as water use and sanitation practices were discussed. The semi-structured interviews were conducted with traditional healers (three in Zouatta II, two in Mélapleu). The roles of traditional healers in the community and common diseases they deal with were discussed. The traditional healers' knowledge of intestinal helminth infections and schistosomiasis was also explored. FGDs and interviews were tape-recorded and transcribed. The information was used to create a detailed reconstruction of villagers' KAP pertaining to intestinal schistosomiasis and soil-transmitted helminthiasis. Quantitative methods Quantitative techniques consisted of household surveys that utilized a structured questionnaire with both closed and open-ended questions. Closed questions pertained to demographic and socio-economic factors, knowledge of local terms for schistosomiasis, and measures for preventing parasitic worm infection. Other aspects of knowledge and practices were explored by open-ended questions. A complete list of households in each village was obtained by census and all households were enrolled. Only household heads were interviewed; if a household head was absent, an adult household member was interviewed instead. Questionnaires were administered in the local language by trained enumerators. The survey collected demographic data and assessed interviewee's knowledge and practices of parasitic worms. Because there is no local translation for intestinal schistosomiasis, we inquired about related symptoms, such as blood in stool and abdominal pain [25], [39]. Respondents were asked whether they consider intestinal worms and schistosomiasis harmful, how an individual becomes infected, type of treatment sought, how to avoid worm infections, and the source of information. Socio-economic status A household-based asset approach was used to estimate the socio-economic status of each household, including principal component analysis [40]. The first principal component (PC) of asset ownership across households explained 20% of the variability and gave greatest weight to households possessing a radio (0.47), followed by a ventilator (0.42), and a television (0.42). After standardization of these weighted asset variables, households possessing a ventilator had the greatest score (1.57), followed by households with a refrigerator (1.53). The lowest scores were associated to households that lacked a bicycle (−0.47) or a radio (−0.38). The asset scores were summed to a total score attached to each household, and households were ranked according to their total score. Thereafter, households were grouped into wealth quintiles: most poor, very poor, poor, less poor, and least poor [28], [41]. Data management and analysis Qualitative data analysis was based on the model of systems of signs, meaning, and action [42]. It aims to identify the system of signs, meaning, and actions that contribute to individuals' perceptions, interpretations, and behavior of health. A preliminary analysis was performed on the public perception of helminth infection and then created a “code list”. This code list documents information categories, types, and contents related to public perceptions of a helminth infection. With the help of this code list, interviews and FGDs were broken down into multiple units. Coded interviews and FGDs were then entered into a Maxqda database (VERBI Software Consult, Social Research, Gmbh; Berlin, Germany). The coded data were analyzed for the frequency at which information and content categories occur, including correlations between these variables. The software also allows for the rapid retrieval of text related to one or more information categories and the identification of informants. After coding, the first level of analysis was conducted to identify different types of symptoms, perceived causes, preventative strategies, and treatment options that were outlined by respondents. Water contact behavior and sources of information were identified in the frame of the first level of analysis. The second level of analysis examined the contents of several categories of information by investigating the implied meaning associated with each category. The analysis was also conducted on the articulations and discontinuities among the system of signs, meaning, and actions. Quantitative data were entered into EpiInfo version 6.04 (Center for Disease Control and Prevention; Atlanta, GA, USA). Analyses were performed with STATA version 8.0 (Stata Corporation; College Station, TX, USA). A chi-square (χ2) test was used to determine inter-village differences. χ2 and Fisher's exact tests were used to assess the association between KAP, demographic factors, and socio-economic variables. Ethical statement The study protocol was approved by the institutional research commissions of the CSRS in Abidjan, Côte d'Ivoire and the Swiss TPH in Basel, Switzerland. The study was cleared by the Ministry of Higher Education and Research of Côte d'Ivoire, and the district health and education authorities of Man. The village chiefs in Zouatta II and Mélapleu were asked for permission to work in the village, and then a meeting was organized with the village authorities to explain the aims and procedures of the study. The purpose and activities of the study were explained to the local community including parents and teachers. Sufficient time was given to ask question and it was emphasized that participation was voluntary. Oral consent was obtained, since the majority of the participants were illiterate. A local witness was present during oral consent. Hence, we followed common procedures for studies carried out in Côte d'Ivoire when only questionnaire data are collected and no concurrent biological samples. Results Characteristics of the study population A total of 207 interviews were conducted with household heads; 111 (53.6%) in Mélapleu and 96 (46.4%) in Zouatta II. Table 1 shows the respondents' characteristics. The two communities showed no difference with regard to age, sex, education, and occupation. However, there was a significant difference in religion; the majority of interviewees in Mélapleu were animists, whereas Christians were predominant in Zouatta II. Moreover, marital status differed significantly between the two villages with a higher proportion of married or widowed household heads in Mélapleu than in Zouatta II. 10.1371/journal.pntd.0000910.t001 Table 1 Characteristics of the study populations in western Côte d'Ivoire, subjected to KAP surveys for parasitic worms in 2003/2004. Characteristics Total Village χ2 P-value (n = 207)a Zouatta II(n = 96)a,b Mélapleu(n = 111)a,c Sex Male 57 58 55 Female 44 42 45 0.23 0.625 Age group (years) 18–35 34 29 38 36–60 44 49 39 >60 23 22 55 2.43 0.296 Ethnicity Yacouba 53 3.1 96 Wobé 40 87 0 Others 7.2 10 4.5 N/A 60(n = 18)a Perceived causes Drinking dirty water 86 89 89 77 2.05 0.357 75 90 94 4.67 0.097 Bathing in dirty water 83 82 79 91 1.41 0.493 71 93 78 5.88 0.053 Open defecation in water 71 71 71 68 0.07 0.964 71 71 67 0.15 0.925 Malnutrition 57 63 50 55 1.19 0.549 54 67 39 4.13 0.126 Consumption of dirty fruits 51 55 46 50 0.51 0.772 43 55 56 1.12 0.568 Inborn disease 38 19 7.1 4.5 0.18b 0 12 28 N/A 0.015b Place of treatment Dispensary/hospital 88 84 93 86 1.13 0.566 96 83 83 2.99 0.224 Family 35 50 25 23 6.42 0.04 18 40 50 5.93 0.052 Traditional healer 15 24 7.1 7.1 0.15 0.119 11 9.5 33 N/A 0.045b Type of treatment Pharmaceutical medicine 85 84 96 72 5.55 0.062 86 81 94 1.82 0.401 Traditional medicine 35 55 25 14 N/A 0.002 b 18 40 50 5.93 0.052 Medicine sold on street markets 27 42 18 14 N/A 0.023 b 25 26 33 0.43 0.806 Prevention Avoiding drinking dirty water 89 97 92 71 0.01 0.010 83 90 94 1.46 0.481 Avoiding bathing in dirt water 86 86 80 95 2.28 0.319 96 83 76 3.14 0.208 Avoiding open defecation in water 68 69 80 71 0.99 0.609 74 80 53 4.62 0.099 Avoiding unripe fruit consumption 69 80 68 48 6.31 0.043 50 69 67 2.76 0.251 Data were pooled for the two study villages (Mélapleu and Zouatta II) and stratified by educational attainment and age groups. N/A, not applicable. a All values are percentages. b P-value based on Fisher's exact test. Qualitative data confirmed these findings in terms of prevention, illustrated by the following quote from a 42-year-old man from Mélapleu: “If someone knows the way of the transmission of a disease, he can avoid it. But, we don't know how we contract ‘bilharziose’, therefore we cannot avoid it. I know ‘bilharziose’ from those who went to the hospital and the doctor told them that they had this disease.” Table 7 shows the knowledge, treatment, and prevention among study participants, stratified by wealth quintiles. The poorest quintile mentioned blood in stool as the main symptom of intestinal schistosomiasis and used traditional medicine more often than the least poor. For prevention, the poorest cited avoiding drinking dirty water more often than their wealthier counterparts who, in turn, indicated more frequently to avoid bathing in dirty water. The majority of the participants mentioned that they avoided water contact as a preventive measure. 10.1371/journal.pntd.0000910.t007 Table 7 Knowledge of signs and symptoms, perceived causes, treatment, and prevention of schistosomiasis, stratified by wealth quintiles, in 2003/2004. Variable Totala Wealth quintile Ratio(most poor/least poor) Most poora Very poora Poora Less poora Least poora Knowledge of schistosomiasis (n = 207) 43 23 20 20 15 22 1.03 Signs and symptoms (n = 88) Blood in stool 93 100 89 94 92 89 1.11 Blood in urine 86 90 83 83 85 89 1.00 Abdominal pain 81 80 83 78 77 84 0.95 Vomiting 75 90 78 67 62 74 1.22 Diarrhea 73 70 83 72 69 68 1.02 Dysentery 38 55 28 28 38 37 1.49 Perceived causes Drinking dirty water 86 90 83 89 92 79 1.14 Bathing in dirty water 83 90 83 83 77 79 1.14 Open defecation in water 71 90 67 78 38 68 1.31 Malnutrition 57 63 72 61 38 42 1.49 Consumption of dirty fruits 51 60 56 44 46 47 1.22 Place of treatment Dispensary/hospital 88 90 78 83 92 95 0.95 Family 35 40 50 39 13 26 1.34 Traditional healer 15 10 22 28 7.6 5.2 1.92 Type of treatment Pharmaceutical medicine 85 80 78 83 92 95 0.84 Traditional medicine 35 55 44 33 18 21 2.61 Drugs sold on street markets 27 25 22 39 23 26 0.90 Preventionb (n = 80) Avoiding drinking dirty water 89 85 83 83 85 74 1.15 Avoiding bathing in dirty water 80 75 83 83 69 84 0.89 Avoiding open defecation in water 74 75 83 67 46 58 1.29 Avoiding unripe fruit consumption 69 65 78 50 77 47 1.37 Source of information Hospital 61 70 61 44 85 53 1.33 Health workerc 59 65 61 56 69 42 1.54 Radio 51 55 56 33 62 53 1.04 Television 48 45 50 44 38 58 0.77 Family 35 35 28 50 38 26 1.33 School 26 30 17 22 31 32 0.95 Traditional healer 11 10 0 17 7.6 16 0.63 Data from the two study villages (Mélapleu and Zouatta II) in western Côte d'Ivoire were pooled. a All values are percentages. b Only people who gave an affirmative response for prevention were included in this analysis. c Schistosomiasis project staff. Water contact behavior Table 8 summarizes the principal reasons for water contact. We observed that pumps supplying potable water in each community were broken, and hence access to clean drinking water was difficult. The most frequent domestic activities placing individuals in contact with contaminated water were bathing in rivers, washing clothes, and crossing rivers. In each village, significant differences were found for washing dishes, bathing children, fetching drinking water, farming, fishing, swimming, and playing (all P<0.05). 10.1371/journal.pntd.0000910.t008 Table 8 Reasons for water contact among respondents, stratified by study village, in 2003/2004. Reason for water contact Total(n = 207)a Village χ2 P-value Zouatta IIa,b(n = 96) Mélapleua,c (n = 111) Bathing 92 89 96 3.49 0.062 Washing clothes 91 93 90 0.44 0.505 Crossing rivers 65 72 59 3.49 0.061 Washing dishes 65 51 77 14.7 <0.001 Washing children 65 44 82 34.5 <0.001 Fetching water 56 43 67 12.0 0.001 Fishing 53 62 45 6.29 0.012 Swimming 38 51 27 12.6 <0.001 Farming 21 14 28 6.36 0.012 Playing 6.3 10 3.0 5.20 0.023 Religious practices 3.9 3.0 5.0 0.26 0.608 a All values are percentages. b Village subjected to community-based research and control activities. c Village subjected to school-based research and control activities. Data from non-participant observation revealed that water contact patterns were similar in both villages. Rivers are frequently used for both occupational and recreational activities. Some women mentioned that they preferred to wash clothes in rivers because suitable washing stones were available and there was time for social interaction and community chores. We observed water contact behavior in both villages that could lead to contamination, such as women washing clothes, fishing, and children bathing in the river simultaneously. Moreover, we found evidence of open defecation along riverbanks. Discussion The aim of this study was to deepen our understanding and compare the local KAP of parasitic worm infections in two rural communities of western Côte d'Ivoire that were subjected either to school-based (Mélapleu) or community-based research and control activities (Zouatta II) against intestinal schistosomiasis and soil-transmitted helminthiasis. Both qualitative and quantitative methods were employed and data were triangulated. Since heads of households are a strong and recognized component of the cultural and social setting [43], [44], special emphasis was placed on interviewing these individuals. Demographic and socio-economic profiles in the two villages were similar with the exception of ethnicity, religion, and marital status. Interestingly, when household heads were asked about health problems within the household and the community in general, intestinal worms and schistosomiasis were rarely mentioned spontaneously as a health problem of prime importance. This observation does not suggest that these infections are negligible, since worms were mentioned to be a serious health problem upon further probing. Most of the household interviewees possess more detailed knowledge of how a worm infection occurs and what measures are available for prevention than for schistosomiasis. The term ‘bilharziose’ was more readily understood in Zouatta II than in Mélapleu, although there was only little knowledge on the mode of transmission and how to prevent schistosomiasis, even in Zouatta II. Our analysis of people's representations and practices against worms revealed that knowledge and practices lacked clear linear relationships. The following two considerations are offered for discussion. First, schistosomiasis and soil-transmitted helminthiasis are deeply engrained in social-ecological systems [45], and hence the way of life and common behaviors are difficult to change. For example, open defecation was said to be more comfortable than in latrines. With regard to water supply, the water from unprotected open sources was reported to be of better taste compared to that from wells. Second, there was a lack of alternatives for the clean drinking water and improved sanitation. For example, the pumps which would have provided safe drinking water were not functional in the two villages at the time of the survey, and only one out of four households surveyed had latrines. Previous studies carried out in other schistosome-endemic areas found a comparatively higher level of awareness of schistosomiasis than was observed in these two villages of western Côte d'Ivoire. For example, Ndamba (1998) reported that 80% of villagers in Zimbabwe were aware of schistosomiasis [46]. In a community in south-eastern Nigeria, 42% of respondents had a clear perception of the disease and 27% were aware of high prevalence rates [47]. Prior research conducted in Brazil [22] and Egypt [48] revealed that people were fairly familiar with schistosomiasis. It is conceivable that the better knowledge of intestinal schistosomiasis in Zouatta II than in Mélapleu is attributable to the health information conveyed through a community-based approach. Indeed, respondents from Zouatta II mentioned that research and control activities served as their main source of information. Moreover, some villagers noted that information on schistosomiasis was passed on to them through family members, thus indicating that community social organizations may act as an intermediary to deliver health education messages. A Senegalese study [49] demonstrated lower awareness of intestinal schistosomiasis among the population despite several years of health education, using a diversity of communicational outlets, including radio, television, and posters, among others. Lessons learned in Senegal point out that a research project can have a positive effect on raising local knowledge, and it was concluded that intensive community-based actions are an effective means to do so. As participants from Mélapleu said that they learned about disease transmission at school, including and further strengthening the role of teachers in health education and community health promotion should be envisaged. Both the school and community structures should be integrated in such a health education program, so that school children can act as agents for the diffusion of health education messages. Indeed, studies from Brazil indicate that schools are a key source of information for schistosomiasis [22]. Passive case detection may be considered as a potential control measure if drugs are available at local and regional health facilities. An important mechanism to enhance health outcomes is to teach local community members (e.g., community health workers and teachers) about the signs and symptoms of worm infection, and implementing a community outreach treatment and prevention program. With this type of control strategy, however, community perceptions of diseases are particularly important in ensuring the control strategy's effectiveness, as perception will affect compliance [50]. In fact, recent evidence suggests that in the north-western part of Uganda communities are increasingly resisting to regularly take anthelmintic drugs as part of preventive chemotherapy programs targeting multiple neglected tropical diseases simultaneously [51]. In our study, treatment by passive case detection should be considered as most of the respondents trusted pharmaceutical drugs. However, people used both modern and traditional medicine to treat worm infections; the majority of them considered modern medicine to be inaccessible, and used traditional medicine or drugs sold on local markets. This is consistent with findings from a study in Egypt, where it was found that traditional medications were frequently used, since modern treatments were either unavailable due to high costs or lack of supply [48]. With regard to the transmission of parasitic worms, a common belief in our study villages was that this primarily was through food. In particular, consumption of meat, sweets, and over-ripe fruits were perceived as key factors in disease transmission. The relationship between consumption of specific foodstuffs and intestinal helminth infections likely relates to the associated abdominal symptoms. For example, consumption of spoiled meat or over-ripe fruits is thought to cause symptoms of bloating and cramping, similar to helmintic infections. Curtale and colleagues [52] made similar observations in Egypt, where a close association between food and helminth infection was established. The perception relating food with helmintic disease affected the behavior of the current study populations regarding protective measures. In many instances, children with helminth infections were not allowed to consume either meat or fruit. From a public health perspective, this is an important issue as these food items are of high nutritional value. Hence, restricting certain foodstuffs as they are perceived to be associated with helmintic infection may lead to, or further exacerbate, delayed child development [21], [53], [54]. Furthermore, our quantitative results revealed that soil was an unknown source of transmission for intestinal worm infections. This was confirmed during FGDs; only one woman in a FGD mentioned that infection could be transmitted when children eat soil. With regard to intestinal schistosomiasis, we did not identify any particular beliefs within the communities. This finding is in contrast to urinary schistosomiasis; common beliefs such as hematuria have been reported as a sign of puberty for male individuals [55]. Nonetheless, the observed low awareness of intestinal schistosomiasis in an area of high endemicity is intriguing, and clearly demonstrates the difficulty in comparing the biomedical and popular conception of disease. In fact, intestinal schistosomiasis is frequently confused with other diseases that have the same or similar symptoms. In general, there seems to be a lack of consistency between the transmission and preventive measures taken against schistosomiasis and other parasitic worm infections. Commonly, people's knowledge is a combination of endogenous and exogenous wisdom. Indeed, respondents gave answers in both categories; there was knowledge with a clear biomedical root obtained from health workers and the research team on one hand, and information obtained from the cultural milieu on the other hand. For example, people mentioned that wearing shoes is a preventive measure against worms, without mentioning that soil contact is necessary for worm transmission. The knowledge of shoes preventing soil-transmitted helminth infections was obtained or reinforced by the research team during the meetings preceding the 2004 survey. It follows that knowledge of the modes of transmission and prevention of worm infections was moderate at best. Improving the public's perception of schistosomiasis would require sustained control efforts and intensive educational actions. Yet, enhanced knowledge and practices do not necessarily lead to behavioral changes. For example, even if the public's awareness about infection risks improves, people will continue to visit contaminated water sources if there are no readily available alternatives, the fetching of water at open water sources continues to be related to important social interaction, and the taste of current water sources is perceived as better than the water obtained from wells [56]–[58]. Hopefully following a community-based health education campaign, knowledge of common symptoms and transmission may lead to improved health-seeking behavior and early treatment [59], [60]. We found two health-conscience behaviors, namely hand washing before eating and hand washing after defecation. While these behaviors are laudable, they are unfortunately overshadowed by other practices of poor hygiene. For example, only 25% of households had a latrine and despite this, villagers tend to defecate where convenient – still rarely using latrines where available. Such practices are dangerous as the number of helminth eggs produced by one adult female worm is so large that a single contaminated stool passed in the soil is sufficient to infect an entire village [61]. It would be interesting to try a community-led total sanitation approach (CLTS) and measure the impact of such a strategy on re-infection patterns of soil-transmitted helminthiasis, intestinal schistosomiasis and other neglected tropical diseases [17]. CLTS is an integrated approach to achieve and sustain an open defecation-free status of communities through a participatory approach. It facilitates the critical analysis by the community of their own sanitation profile, their practices of defecation and the consequences, leading to collective action to become open defecation-free, and hence is accompanied by environmental measures to improve sanitation, hygiene practices, waste disposal, and protection of clean drinking water sources [62]. In conclusion, our results emphasize that current morbidity control through preventive chemotherapy primarily targeting school-aged children has limitations. Older population segments are insufficiently addressed, and hence new knowledge on prevention and control of parasitic worm infections is minimal. Improved access to clean water and sanitation is necessary for sustainable control of major helminthiases, and participatory approaches such as CLTS should be attempted. Our results further suggest that educational programs should target areas of high endemicity with community-based interventions. We recommend that household heads from all socio-economic segments should be specifically targeted, so that they can transmit important health information to their children and relatives. For such a program to be effective, a continuous surveillance process directed at monitoring passive case detection, assessing the impact of health education messages, and evaluating change in infection patterns are necessary. Supporting Information Alternative Language Abstract S1 Translation of the abstract into French by Cinthia Acka (.27 MB DOC) Click here for additional data file. Alternative Language Abstract S2 Translation of the abstract into German by Jürg Utzinger and Jennifer Keiser (.28 MB DOC) Click here for additional data file. Alternative Language Abstract S3 Translation of the abstract into Italian by Giovanna Raso and Aurelio Di Pasquale (.27 MB DOC) Click here for additional data file.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                25 November 2015
                2015
                : 10
                : 11
                : e0143667
                Affiliations
                [1 ]Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
                [2 ]Azal National Research Center, Azal University for Human Development, Sana’a, Yemen
                [3 ]Department of Parasitology, Faculty of Medicine and Health Sciences, Sana’a University, Sana’a, Yemen
                [4 ]Department of Biology, Faculty of Natural and Applied Sciences, Umaru Musa Yar’adua University, Katsina, Katsina State, Nigeria
                Tulane University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HMA II JI AA. Performed the experiments: SD AMA HS NAN WMA. Analyzed the data: SD HMA. Wrote the paper: SD HMA II.

                Article
                PONE-D-15-36777
                10.1371/journal.pone.0143667
                4659601
                26606264
                7f4987ab-89df-4858-87e0-f4933578df55
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 20 August 2015
                : 6 November 2015
                Page count
                Figures: 1, Tables: 5, Pages: 14
                Funding
                The work presented in this paper was funded by the University of Malaya High Impact Research Grant UM-MOHE UM.C/625/1/HIR/MOHE/MED/18 from the Ministry of Higher Education Malaysia, and also by the University of Malaya Research Grants; RG331-15AFR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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