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      Prevalence of Soil-Transmitted Helminth and Schistosoma mansoni Infection and Their Associated Factors among Hiruy Abaregawi Primary School Children, Rural Debre Tabor, North West Ethiopia: A Cross-Sectional Study

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          Abstract

          Background

          In Ethiopia, 25.3 and 12.3 million school-age children are living in soil-transmitted helminth and schistosomiasis endemic areas, respectively. The school children are at risk for both soil-transmitted helminths and Schistosoma mansoni due to juvenile activities like walking barefoot, playing with dirty objects that might be contaminated with feces, and fetching of unclean water for drinking. There are no data that indicate the status of soil-transmitted helminths and Schistosoma mansoni among children at Hiruy Abaregawi primary school. Therefore, the main objective of this study was to determine the prevalence of soil-transmitted helminth and Schistosoma mansoni infection among Hiruy Abaregawi primary school children.

          Methods

          A cross-sectional study was conducted from March to April, 2019, at Hiruy Abaregawi primary school, Rural Debre Tabor, North West Ethiopia. A total of 340 students were included in the study. Informed written consent was obtained from the children's parent. Systematic sampling technique was used to select the children. About 2 grams of stool samples was collected and transported to Debre Tabor University Microbiology and Parasitology Teaching Laboratory to conduct the Kato-Katz technique. Data were analyzed using SPSS version 23. Variables with a p value < 0.05 were considered statistically significant.

          Results

          The prevalence of soil-transmitted helminths and Schistosoma mansoni was 51/340 (15%). Among the identified parasites, Ascaris lumbricoides accounts for 28 (8.2%), hookworm 13 (3.8%), Trichuris trichiura 4 (1.2%), and Schistosoma mansoni 6 (1.8%). In this study, 24 (7%) of Ascaris lumbricoides-, 11 (3.2%) of hookworm-, 4 (1.2%) of Trichuris trichiura-, and 5 (1.5%) of Schistosoma mansoni-infected children showed light infections and no heavy infection in both soil-transmitted helminths and Schistosoma mansoni was observed. Finger nail trimming status, hand washing before eating, availability of toilet at home, educational level of students, and sex of students were factors associated with soil-transmitted helminth infection. Conclusion and Recommendations. In this study, the low prevalence of soil-transmitted helminths and Schistosoma mansoni was observed. The combination of regular mass deworming program and health information on risk factors should be strengthened for the prevention and control of soil-transmitted helminth infection.

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          Most cited references13

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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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            Prevalence of intestinal helminthic infections and malnutrition among schoolchildren of the Zegie Peninsula, northwestern Ethiopia.

            A cross-sectional study involving 408 schoolchildren was performed from November 2013 to February 2014 to assess the prevalence of intestinal helminthic infections and malnutrition among schoolchildren of the Zegie Peninsula, northwestern Ethiopia. A structured questionnaire was used to gather data on the demographic and risk factors associated with intestinal helminthic infections. Stool samples were collected and examined for helminth eggs using the formalin-ether concentration technique. In addition, anthropometric measurements were performed to assess the nutritional status of the schoolchildren. The overall prevalence of intestinal helminthic infections in the study area was 69.1%. Single, double, triple, and quadruple infections were 42.2%, 18.4%, 5.9%, and 0.7%, respectively. The prevalence of hookworm, Schistosoma mansoni, Ascaris lumbricoides, Trichuris trichiura, Hymenolepis nana, and Strongyloides stercoralis infections were 43.4%, 29.9%, 12.7%, 10%, 4.6%, and 0.7%, respectively. The prevalence of malnutrition in terms of stunting, being underweight, and wasting were 15.3%, 18%, and 27.6%, respectively. However, no significant association was found between intestinal helminthic infections and stunting, being underweight and wasting (p>0.05). It can be concluded that intestinal helminthic infections, specifically infections due to hookworm and S. mansoni, are important health problems among schoolchildren of the Zegie Peninsula.
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              Nigeria: “Ground Zero" for the High Prevalence Neglected Tropical Diseases

              Among all of the African nations, Nigeria has the greatest number of people infected with neglected tropical diseases (NTDs). With the right political will, the country has sufficient resources to expand its current investments for the important work of Nigeria's NTD program. In a 2009 analysis of the NTDs in sub-Saharan Africa, one of us identified Nigeria as the country with the greatest number of cases of the so-called high prevalence NTDs, such as the intestinal helminth infections, schistosomiasis, and lymphatic filariasis (LF) [1]. Shown in Table 1 is a list of the major NTDs that can be targeted for integrated NTD control and/or elimination, which also includes onchocerciasis. The information confirms that Nigeria has the greatest number of intestinal helminth infections, i.e., ascariasis, hookworm, and trichuriasis, among all African nations, ranking fourth or fifth globally behind only the much higher populated middle-income Asian nations, such as China, India, and Indonesia [1]–[4]. Nigeria also has the greatest number of cases of schistosomiasis worldwide, with both intestinal schistosomiasis caused by Schistosoma mansoni and the urogenital schistosomiasis caused by Schistosoma haematobium endemic to that country [1], [5]. In terms of the high prevalence vector-borne NTDs, Nigeria has the greatest number of cases of LF and onchocerciasis in Africa, ranking globally third and first, respectively, and accounting for one-fourth or more of the global disease burden from these two NTDs [6]–[9]. Nigeria also has an estimated 18 million people at risk for trachoma, with nearly 1.3 million people living with trichiasis [10], and the third or fourth largest number of new cases of leprosy in Africa (behind Ethiopia and the Democratic Republic of Congo) [11], in addition to some of the greatest number of cases of the lower prevalence NTDs, including yellow fever, rabies, and Buruli ulcer in Africa [1]. The World Health Organization (WHO) reports that there may be 21 “alleged" or “suspected" remaining cases of dracunculiasis in Nigeria [12], although it is widely accepted that transmission of guinea worm has been interrupted there. 10.1371/journal.pntd.0001600.t001 Table 1 Ranking of Nigeria by neglected tropical diseases cases and prevalence. Disease Estimated Number of cases in Nigeria Ranking in Africa Percentage of Global Disease Burden Ranking Globally Reference Ascariasis 55 million 1 7% 5th behind India, Indonesia, China, and Bangladesh [1]–[4] Hookworm 38 million 1 7% Tied for 4th with China behind India, Indonesia, and Bangladesh [1]–[4] Trichuriasis 34 million 1 6% 4th behind India, Indonesia, and Bangladesh [1]–[4] Schistosomiasis 29 million 1 14% 1 [2], [5] Lymphatic filariasis • 25 million• 80–121 million estimated at risk, requiring mass drug administration 1 21% 3rd [6]–[8], [27] Onchocerciasis 30 million at risk, requiring mass drug administration 1 36% 1 [6], [9] Trachoma 18 million at risk Not determined Not determined Not determined [10] Leprosy 4,531 registered prevalence 4 2% 7th [11] The high prevalence NTDs are responsible for an enormous disease burden in Africa, equivalent to almost one-half the disease burden from malaria when measured in disability-adjusted life years [1]. There is an equally important adverse economic impact because of the effects of these NTDs on maternal-child health and worker productivity in Africa [1]. However, the seven most common NTDs can often be controlled or in some cases even eliminated through low cost “rapid-impact" packages of drugs, which are either donated by multinational pharmaceutical companies or through the purchase of low-cost generic drugs. At a cost of less than US$1 per person annually, the prevalence of the intestinal helminth infections and schistosomiasis could be reduced in some areas, while LF, onchocerciasis, and trachoma might even be eliminated over a period of several years. Therefore, based on Nigeria's current population estimate of approximately 150 million people [13], we estimate that such goals could be achieved in Nigeria for significantly less than US$100 million annually. Because the seven high prevalence NTDs have been shown to actually cause poverty, the economic rate of return for integrated NTD control and elimination would be substantial. The enormous disease and economic burden resulting from the seven high prevalence NTDs persist in Nigeria despite the country's economic capacity to absorb some or all of the costs required for disease control and elimination. Nigeria is the most populated nation in Africa, accounting for approximately 20% of Africa's population (Figure 1, Table 2) [6], [13], [14]. It is also the 8th most populated nation worldwide, roughly equivalent to the population of Bangladesh and Brazil [13], [14], but with a gross domestic product (GDP) and purchasing power parity that ranks it with several western European countries such as Belgium or Sweden [15]. Indeed, Nigeria has the third largest economy in Africa, behind South Africa and Egypt, ranking 32nd globally with a GDP of over US$300 billion [15], [16]. Additional estimates indicate that Nigeria is ranked among the top 20 countries globally for foreign direct investments [17]. Moreover, Nigeria is currently experiencing enormous economic growth, which exceeded 8% in 2010 [18], [19], and was almost 7% in 2011 [19]. 10.1371/journal.pntd.0001600.g001 Figure 1 Location of Nigeria. From CIA – The World Factbook (https://www.cia.gov/library/publications/the-world-factbook/geos/ni.html), accessed 1 February, 2012. 10.1371/journal.pntd.0001600.t002 Table 2 Facts and figures about Nigeria. Category Number Ranking Countries with Comparable Ranking Reference Population • 152 million (2010)• 165 million (projected in 2015) 8 Bangladesh And Brazil [13], [14] GDP (purchasing power parity) 378 billion (2010) 32 Belgium andSweden [15] Ranking of economy in Africa 3 Behind South Africa and Egypt [15], [16] HDI (Human Development Index) 0.470 (2005) 158 Eritrea andTanzania [22] Increasingly, much of Nigeria's economic growth depends on oil and other fossil fuels. Today, Nigeria ranks 15th globally in world oil production and 5th in oil exports, in addition to 11th in natural gas exports [20]. The excessive dependence on fossil fuels has created a structural imbalance and lack of diversification leading to high youth unemployment and widespread insecurity [18]. The term “resource curse" has been applied to countries such as Nigeria that have enormous natural resources but underperform with respect to their human development index (HDI) and other metrics linked to a robust economy [21]. Indeed, despite its wealth, Nigeria ranks only 158th in terms of its HDI [22], and so far the country has been unable to meet its Millennium Development Goals (MDGs), including MDG 6 for combating HIV/AIDS, malaria, and other diseases [13]. Additionally, between the years 1990 and 2006, Nigeria regressed in several developmental indices, notably the percentage of its population that had access to safe water coverage and basic sanitation. As of 2006, a majority of Nigerians lack access to safe water coverage (53%) and sanitation (70%) [23]. This situation is not unique to Nigeria, but unfortunately is common among many African nations. The good news is that Nigeria has made some important strides in NTD control and elimination [6], [24]. Some of these successes were accomplished in collaboration with the WHO, UNICEF-Nigeria, and the Atlanta-based Carter Center and its Nigerian offices in Jos, as well as other non-governmental developmental organizations (NGDOs) [6], [8], [24], [25], [26]. The clearest public health victory has been with respect to guinea worm (dracunculiasis) eradication. In 1986, Nigeria accounted for approximately 75% of the world's 3.3 million cases of dracunculiasis. Through investments by the Nigerian government that exceeded US$2 million, in addition to other public and private support, transmission of guinea worm has been halted since 2009 [6]. In addition, with support from the International Trachoma Initiative (ITI), the Nigeria national program has received more than 4.7 million Zithromax treatments since 2010 [10]. In 2011, Nigeria was scheduled to treat 3.1 million people [10], or possibly as many as 5 million [27]. Moreover, in collaboration with the African Programme for Onchocerciasis Control (APOC), the Nigerian Federal Ministry of Health has ensured that more than 96% of 35,000 Nigerian communities at risk for river blindness have received or still receive annual community-directed treatments with ivermectin (CDTI) [24] (Figure 2). These activities have occurred through support of the APOC Trust Fund, NGDOs, and the Nigerian government [24]. Outcomes of recent epidemiological assessments conducted with support from APOC indicate that onchocerciasis transmission has been halted in foci in Ebonyi, Kaduna, and Zamfara states [27]. For onchocerciasis and the other high prevalence NTDs, including LF, schistosomiasis, and trachoma, some of the most notable gains have occurred in the states of Plateau and Nasarawa, where the Carter Center maintains active programs of mass drug administration [6], [25], [26]. As a result, there has been a 95% reduction in onchocercal nodules in these two states, and an 83% reduction in the prevalence of LF [6], [25], [26]. Moreover, praziquantel mass drug administration for schistosomiasis is being integrated with LF and onchocerciasis control and elimination efforts, with targeted praziquantel treatment for schistosomiasis now ongoing in six states [6], [8], [27] (Supporting Document S1). 10.1371/journal.pntd.0001600.g002 Figure 2 Map of Nigeria. From CIA – The World Factbook (https://www.cia.gov/library/publications/the-world-factbook/geos/ni.html), accessed 1 February, 2012. Despite these victories and accomplishments, much of the Nigerian population still lacks access to essential medicines for the high prevalence NTDs. Beginning in 2009, a national program for NTD control and elimination was initiated to promote integrated control nationally. The NTD program of the Nigerian Federal Ministry of Health currently addresses the following diseases: LF, onchocerciasis, schistosomiasis, soil-transmitted helminth infections, trachoma, leprosy, Buruli ulcer, human African trypanosomiasis, and guinea worm disease. The strategy of the NTD program is to progressively reduce morbidity, disability, and mortality due to NTDs using integrated and cost-effective approaches with the goal to eliminate NTDs in Nigeria by the year 2020 [27]. Nigeria has sufficient wealth and resources in order to build on its past successes and embark on an expanded and aggressive program of national disease control and elimination for its highest prevalence NTDs. Costing less than 0.1% of its GDP annually, the program would be comprised of integrated mass drug administration efforts to target the intestinal helminth infections, schistosomiasis, LF, and onchocerciasis, possibly together with administration of long-lasting insecticide-treated nets to also target malaria and LF, as well as the SAFE (surgery, azithromycin antibiotics, facial cleanliness, and environmental control) strategy for trachoma elimination. Through its long-standing collaborations with international agencies such as APOC, WHO, and UNICEF, as well as CBM, ITI, the Carter Center, Helen Keller International, Sightsavers International, Mission to Save the Helpless (MITOSATH), and other NGDOs, the Nigerian Federal Ministry of Health has acquired deep and lasting technical expertise in order to ensure such expanded activities are conducted at maximal efficiencies, minimal costs, and with adequate monitoring and evaluation. A key component would include accelerated mapping of NTDs in Nigeria [28], including an ongoing partnership with the Swiss Tropical and Public Health Institute [29]. A national program of NTD control and elimination, coupled with increased access to clean water and sanitation, would simultaneously serve to strengthen health systems in many of the more fragile Nigerian states, and would represent a highly effective pro-poor strategy for Nigerian President Goodluck Jonathan in his first elected term. Doing so would be an appropriate activity for a nation currently undergoing its longest period of civilian rule since independence and one recently awarded a seat on the United Nations Security Council [30]. There is also an urgent need for new and improved control tools for Nigeria's NTDs, including the development of a new macrofilaricide for onchocerciasis and other medicines, simpler and less expensive diagnostic reagents, and NTD vaccines [6]. In parallel with expanded disease control and elimination efforts, Nigeria's best universities and research institutes must expand their research and training capacity for NTDs. Several Nigerian capacity-building and partnering programs with institutions in the United States and United Kingdom are already in place, including one between the Nigeria's National Academy of Science together with the US National Academies through the African Science Academy Development Initiative (ASADI) [31], and between the University of Ibadan (in partnership with several other Nigerian universities) and two US universities (Northwestern University and Harvard School of Public Health) through the Medical Education Partnership Initiative in Nigeria (MEPIN) supported by the US National Institutes of Health [32], but these too could be expanded. A Nigeria free from its high prevalence NTDs can be expected to accelerate that nation's economic development through improvements in child growth, intellect and cognition, pregnancy outcome, and worker productivity. Through expansions in integrated NTD control and disease elimination, Nigeria would become an important role model for all of Africa. Supporting Information Supporting Document S1 “Brief on NTD," unpublished document by Nigerian Ministry of Health, received January 24, 2012. (DOC) Click here for additional data file.
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                Author and article information

                Contributors
                Journal
                J Parasitol Res
                J Parasitol Res
                JPR
                Journal of Parasitology Research
                Hindawi
                2090-0023
                2090-0031
                2020
                29 January 2020
                : 2020
                : 2521750
                Affiliations
                Debre Tabor University, College of Medicine and Health Sciences, Department of Medical Laboratory Science, Debre Tabor, Ethiopia
                Author notes

                Academic Editor: Bernard Marchand

                Author information
                https://orcid.org/0000-0003-0137-3426
                https://orcid.org/0000-0002-3107-4833
                https://orcid.org/0000-0001-5984-4281
                Article
                10.1155/2020/2521750
                7204315
                0545ca7c-bb76-4f59-964f-9a9243fd72f5
                Copyright © 2020 Lemma Workineh et al.

                This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 5 August 2019
                : 6 November 2019
                : 26 December 2019
                Categories
                Research Article

                Parasitology
                Parasitology

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