https://orcid.org/0000-0002-4658-6532
Figures
Abstract
Background
Schistosomiasis is a parasitic infection that causes significant public health problems in tropical countries. Schistosoma haematobium species are blamable for causing urinary schistosomiasis. The infected person, specifically children, may be carrying the disease. This systematic review aimed to identify the current knowledge of urinary Schistosmiasis in children or USC on its epidemiology, risk factors, and challenges to spread the understanding of controlling the disease and reducing the complications.
Method
In November 2021, a systematic computer-aided literature review was conducted using PubMed, SCOPUS and Web of Science, following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) criteria. The results were updated in February 2022. We only used papers that have at least the abstract available in English. Relevant articles were screened, duplicates were deleted, eligibility criteria were applied, and studies that met the criteria were reviewed. The keywords Human Schistosoma infections, prevalence, risk factors and challenges were included. The protocol for the review was registered with PROSPERO (registration number CRD42022311609). Pooled prevalence rates were calculated using the programme R version 4.2.1. Heterogeneity was assessed using the I2 statistic and p-value. A narrative approach was used to describe risk factors and challenges. Studies were selected and finalised based on the review question to prioritise. The quality of the included studies was assessed using the Mixed-Method Appraisal Tool (MMAT).
Results
A total of 248 publications met the requirements for inclusion. Fifteen articles were included in this review, with the result showing high heterogeneity. The pooled prevalence of urinary schistosomiasis in children is 4% (95% confidence interval (CI)). Age, poor socioeconomic status, education, exposure to river water, and poor sanitation are the risk factors identified in this review. Challenges are faced due to limitations of clean water, lack of water resources, and poor hygiene.
Conclusion
Modifiable risk factors such as poor knowledge and practices must be addressed immediately. Healthcare providers and schools could accomplish engaging in practical promotional activities. Communicating the intended messages to raise community awareness of urinary schistosomiasis is critical.
Citation: Masdor NA, Kandayah T, Amsah N, Othman R, Hassan MR, Rahim SSSA, et al. (2023) Systematic review with meta-analysis: Prevalence, risk factors, and challenges for urinary schistosomiasis in children (USC). PLoS ONE 18(8): e0285533. https://doi.org/10.1371/journal.pone.0285533
Editor: Clement Ameh Yaro, University of Uyo, NIGERIA
Published: August 17, 2023
Copyright: © 2023 Masdor et al. 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.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Unfunded studies.
Competing interests: NO authors have competing interests.
Introduction
Schistosomiasis is a parasitic infection with serious public health consequences in tropical countries [1,2]. This disease has infected 240 million people and 133.3 million preschoolers. Schistosoma haematobium species is blamable for causing urinary schistosomiasis, which occurs in Africa, Turkey, and India [3].
Cercariae from Bulinus snails act as an intermediate host in infected water that penetrates the human skin. Adult schistosomes travel to the bladder’s vesicular and pelvic venous plexus then Females deposit eggs in the bladder and ureters. Some parasite eggs are expelled, while others might build up in bladder tissues, causing ulceration, hematuria, and UTI symptoms [4]. The life cycle of Schistosoma haematobium in freshwater is shown in S1 Fig.
The infected child may unknowingly be carrying the infection. The diagnosis is based on the detection of eggs under a microscope. Infection is also indicated by the presence of antibodies and/or antigens in blood or urine samples. The standard diagnostic technique is filtration using nylon, paper, or polycarbonate filters. Chemical reagent strips can detect microscopic blood in children’s urine if they exhibit hematuria [4]. Chronic active or chronic late urinary schistosomiasis is diagnosed using ultrasound. For mass screening, detecting worm antigens, DNA, and specific antibodies is prohibitively expensive [5]. If left untreated, chronic irritation in the bladder may result in iron deficiency anaemia, malnutrition, impaired development, and a higher risk for bladder cancer later in life [6].
The risk of infection is linked to demographic characteristics [such as age, sex, and occupation) and environmental factors [7]. The USC intermediate host snail prefers still or slow-moving bodies of water, such as lakes. Some residences lack bathrooms, and in Africa and Asia, open defecation is common, contaminating water bodies with infectious faeces [8]. As a result, the infection affects more underprivileged and poor rural groups, particularly women and people in agriculture and fishing areas [4,7].
Children are more susceptible to infection due to poor hygiene and exposure to contaminated water. The age of exposure to infected water is younger in high endemic areas and may become more frequent as age increases due to multiple visits [9]. The other important risk factors include parents and caregivers [7],who bring their child swimming, fishing, and animal bathing as an outdoor activity [10]. Although school children are taught to avoid contaminated water, the lack of choices drives their contact with infected water.
Other known barrier to eliminating schistosomiasis is a lack of safe water provided by the government [11]. Shortage of piped water supply forces communities to rely on freshwater sources for domestic, school, and recreational purposes. The school project initiative provides rainwater-harvesting tanks for all public schools in Kenya [12] as alternative, but the approach did not meet the whole purpose as it only works during the rainy season.
For prevention and controlling schistosomiasis, the World Health Organization (WHO) proposed praziquantel-based preventive chemotherapy given to school-aged children aged 5 to 15 [1]. Over the past few decades, schistosomiasis has been controlled chiefly through mass drug administration (MDA) of praziquantel (PZQ) [13]. However, PZQ has limitations against juvenile schistosomes and cannot prevent re-infection, causing schistosomiasis incidence and transmission to remain unsolved. No schistosomiasis vaccines are currently available [13].
The study on disease prevalence, risk factors and addressing the challenges are fundamental in understanding schistosomiasis. Subsequently, this systematic literature review aims to identify the current knowledge of USC on its epidemiology, risk factors, and challenge to help spread the knowledge in tackling the control of the infection and reducing significant complications of schistosomiasis.
Methods
This review was registered with PROSPERO (registration number CRD42022311609). A literature search was conducted on PubMed, Web of Science and Scopus for studies published from January 2016 to November 2021. To identify and describe the up-to-date evidence of USC, date limitation was used. As a result, we chose the year 2016 as the beginning of the search. In addition, to look for unpublished theses, specific research centres and library sources have been searched.
We used the CoCoPop (Condition, Context, Population) [1] and PECO (Population, Exposure, Comparator, Outcome) research question concepts to determine the inclusion and exclusion criteria. Based on this concept, three main aspects were included: child participants (population), risk factors (exposure) and urinary schistosomiasis (outcome). The three aspects were then combined into one research question:
- What is the prevalence/incidence (Co) of urinary schistosomiasis (Co) in children (P)?
- What risk factors (E) increase the risk of urinary schistosomiasis (O) in children exposed to it (P)? [1]
Terms “trends” or “prevalence” or “epidemiology” “distribution” or “burden” AND “Schistosomiasis” OR “Schistosoma” AND “urinary” OR “bladder” AND “child” or “paediatric” or “kids” AND “risk factors” or “determinants” or “predictors” were used in various combinations as primary search keywords.
The accepted articles were based on the following criteria:
- Study populations that included children under 18 years of age, without restriction of sex or region
- Studies that addressed risk factors associated with urinary schistosomiasis
- Studies that investigated the prevalence and challenges of USC
- All accepted observational and intervention studies, including randomised, quasi-randomised and non-randomised.
All original, primary studies conducted on the epidemiology, risk factors and challenges of urinary schistosomiasis with all full-text English-language published between Jan 1, 2016, to 30 November 2021, qualified to be included in this systematic review.
We excluded articles that did not relate to USC, USC risk factors and prevalence or studies with non-human subjects, study protocols, conference abstracts, dissertations, reviews, qualitative studies, editorials, case studies and opinion articles. Studies with inadequate data on desired information were also excluded. All duplicate studies were deleted, and the full text of the papers was manually and electronically searched using databases.
Screening and selection for inclusion
Firstly, the prescreen was done for study titles and abstracts against the eligibility criteria in phase one. The steps were performed by four reviewers (N.A.M., N.A., T.K. and RO). All reviewers screened for study titles and abstracts independently. Any unrelated articles were removed in this phase. The full texts of the studies identified as potentially relevant in the initial screening were retrieved and screened against the eligibility criteria. After that, four reviewers read the full text independently (N.A.M., N.A., T.K. and RO). Any uncertainty regarding study eligibility was discussed and resolved with another reviewer. Disagreements were resolved through discussion consensus among the five reviewers and input from a lead reviewer.As shown in S2 Fig., a PRISMA-based flow diagram is used to record and illustrate the study selection process at the different stages.
Data extraction
The data from included studies were gathered and documented on a standardised data extraction form by two reviewers (NAM and NA) to document related items and entered in Microsoft Excel with the research information such as authors, year of publication, countries, study design, prevalence, risk factors and challenges. Another reviewer (RO and TK) double-checked the accuracy of the extracted data.
Data synthesis
A narrative approach was used to describe data primarily. The results relevant to the review question were extracted and organised in data extraction form. The studies were chosen and concluded based on the review question in order to prioritise the results summary. This informal method was accomplished by organising the tables and figures used to investigate heterogeneity. The findings include the number of studies and participants, the risk of bias in the studies, the directness of the study addressing the review question and the risk of publication bias to address the certainty of the evidence. The data are presented in tables to compare the findings from included studies. Three independent reviewers (R.O., T.K. and N.A.) double-check the accuracy of the extracted data. To ensure consistency in the results section, all reviewers need to agree on a structure for reporting results.
Data analysis
We performed an initial descriptive analysis of the studies. The I2 statistic was used to assess the heterogeneity of the studies. An I2 value of more than 75% indicates high heterogeneity. As the reported results were very diverse, not all included studies could be used for a meta-analysis. It is excluded if the reviewers conclude that one study is insufficient to add to the evidence base. Pool estimates for prevalence and their 95% confidence interval were obtained with R statistical software version 4.2.1 using the statistical package ’dosresmeta’ by Robert Gentleman and Ross Ihaka of the Department of Statistics, University of Auckland, New Zealand.
Quality assessment of individual studies
The quality of included studies was assessed using Mixed-Method Appraisal Tool (MMAT) assessment [15]. Quality appraisal was conducted using the Mixed Method Appraisal Tool (MMAT). The MMAT evaluates the quality of qualitative, quantitative, and mixed-method studies. It focuses on methodological criteria and includes five core quality criteria for each of the following five categories of study designs: (1) quantitative, (2) qualitative, (3) randomised controlled (4) nonrandomised, and (5) mixed methods. Four reviewers (NAM, NA, TK and RO) independently assessed the quality of the included studies. The reviewers’ discrepancy was managed through discussion, and articles were included after consensus. The quality assessment tool measures a total of nine questions. The highest score from seven questions indicated a low risk of bias. Overall scores of 0–2, 3–5, and 6–7 was declared the low, moderate, and high risk of bias, respectively. The quality assessment is depicted in Table 1.
Results
The search yielded 15 articles from PubMed, 108 from SCOPUS, and 86 from WOS, resulting in 202 unique hits. After rigorous selection screening, only 15 articles were included in the full-text assessment, as shown in the PRISMA flow diagram (S2 Fig). Table 2 present a descriptive summary of the included studies in this review. This systematic review included the findings of 15 studies, as shown in Table 3.
Four articles were from South Africa: two articles from Cameroon, two articles from Nigeria and Sudan, and one article each from Kenya, Malawi, Mauritania, Gambia and Zimbabwe. The articles analysed were published between 2016 and 2021. Fourteen of the 15 articles were cross-sectional studies and one article was a cohort study.
Prevalence of USC
The review found that the prevalence of urinary schistosomiasis among children ranged from 1.82% to 62.0%. The lowest prevalence was in Sudan[14] and the highest was 62% in Nigeria [15].
Risk factors for USC
In four studies included in this review, age was linked to USC [11,14,16–18]. One study found that four-year-old children had a higher risk than two-year-old children [11], and a Sudanese article found that children aged 7 to 10 years old had a higher risk than children aged 10 to 14 years old [14]. Aside from that, four articles [17,19–21] identified gender, particularly boys, as a risk factor in the findings.
Low socioeconomic status and poor education also played significant roles. Children with low socioeconomic status and poor knowledge were more vulnerable to USC than children with higher socioeconomic status [12,15,20]. The child’s current health status, such as stunting, is an important risk factor as the children with stunting had a higher risk of this infection [15,17].
Aside from that, a few articles identified any history of swimming, bathing, lack of clean water, previous exposure to river water [5,19,22] and has non sanitary larine [18] as the contributing factors. Poor hygiene, the presence of other infections such as soil helminth infection [23] and hookworm [12] over a year were also linked to USC.
Seasonal factors such as drought and praziquantel treatment were protective factors and lessened the risk [24]. A relative temperature range of 22–28°C preferable for snails as intermediate hosts [25] will increase the risk of USC.
Challenges in controlling and eliminating USC
Five studies looked at the difficulties of controlling and eliminating USC [5,11,14,16,25].
The most common challenges were a lack of knowledge and information about the disease and the transmission process [11,14]. Most articles in low income countries discuss the limitations of clean water, a lack of water resources, and poor hygiene as challenges in controlling USC [15,25].
All 15 studies have adequate data to perform meta-analysis on prevalence of urinary schistosomiasis. The meta-analysis on the risk factors of urinary schistosomiasis was not possible due to inadequate data. R program version 4.2.1 was used to conduct the analysis. In order to conduct the analysis, articles that reported the prevalence in decimals [1–11] are converted to the nearest whole number to prevent non-integer count error. Random effect model was used to calculate the combined prevalence of urinary schistosomiasis in children. The pooled prevalence of urinary schistosomiasis in children is 4% (95% CI) [2–7]. Heterogeneity was assessed by the I2 statistics versus p-value. A p-value of ≤ 0.05 and I2 ≥ 50% were considered high heterogeneity. The heterogeneity generated was high at 96% and the p-value is less than 0.01 that indicates the test is significant.
Discussion
This study examined the prevalence, risk factors, and challenges in controlling and eliminating USC. Urinary schistosomiasis was prevalent in Sub-Saharan Africa and remained a significant public health concern. Nigeria has the highest schistosomiasis burden in Sub-Saharan Africa, with an estimated 29 million cases of infection [26].
The previous study used MetaXL’s inverse variance heterogeneity model to obtain pooled prevalence estimates (PPE), and this review shows higher PPE for S. haematobium (IVhet PPE: 15%, 95% CI: 6–25) than our review [27]. The low prevalence could be attributed to the fact that the risk group includes children from preschool to 18 years old, as opposed to the previous review, which only included preschool-aged children. Furthermore, schistosomiasis has been primarily controlled through the widespread administration of praziquantel (MDA).
Four studies [11,14,16,17] found that increasing age was associated with urinary schistosomiasis among children. Infection was found in older children aged two to five years, indicating that infection with urinary schistosomiasis occurs early in life because of exposure to contaminated water. School-aged children are more likely to engage in independent water-based play and assist with duties that require contact with water bodies due to their advanced physical and motor development. However, Ugbomoiko et al. observed that the prevalence and intensity of USC over 14 decreased with age [24].
This review identified males as a risk factor for urinary schistosomiasis [14,17,20,25]. Similarly, previous studies showed that boys were more likely to be infected with urinary schistosomiasis than females due to socio-cultural and behavioural factors in which boys are more likely to swim, fish, and play in bodies of freshwater [19,28,29]. Other water-contact activities such as farming, watering cattle and other domesticated animals may result in increased exposure among boys. On the other hand, girls are socially restricted from engaging in water-contact activities such as swimming and bathing. Girls tend to stay home and do housework with tap water, limiting their exposure to other water sources [19].
The occurrence of schistosomiasis was linked to socioeconomic factors. According to Abdulkareem et al., the parent’s unemployment status significantly predicts schistosomiasis [20]. The high unemployment rate in the study area directly indicates low income and poverty. Poverty is linked to several issues, such as poor housing and sanitation, lack of piped water and access to anti-helminths [24].
Poor education may increase the risk of urinary schistosomiasis [30]. This link is most likely interconnected with education influencing attitudes and behaviour in various circumstances. They are more likely to engage in activities that expose them to cercarial penetration, such as crossing a stream or river barefoot. Furthermore, parents’ high illiteracy and negligence, particularly among farmers, can lead to non-education of preventive measures for their children and influence transmission patterns [26]. Stunting has been shown to predict infection with S. haematobium [31]. Stunted children are thought to be more susceptible to parasite infection for various reasons, including a reduction in T-lymphocyte function, defects in antibody synthesis, impaired complement formation, and degeneration of the thymus and other lymphoid tissues.
Climate and ecology have a significant impact on schistosomiasis transmission. During a drought in Ndumo, Kabuyaya et al. reported that S. haematobium declined two years after praziquantel therapy. Ecological and seasonal factors may play a role in schistosomiasis re-infection after treatment. Seasonal/climatic and ecological conditions, such as low rainfall, resulted in continuous drought and the drying up of water bodies (dams) that could have been schistosomiasis hotspots in the study area. Furthermore, drought heatwaves may cause human population concentrations near reservoirs, canals, and rivers, increasing contact with contaminated waterways and the risk of schistosomiasis transmission [16]. The tropical ecology of relative temperatures ranging from 22 to 28°C favours the development of intermediate snail hosts, which will increase the risk of infection [21]. Schistosome intermediate hosts are poikilotherms, which means that their body temperature fluctuates. Temperature influences reproduction, survival, dissemination, and parasite development within the snail. Climate change may alter the distribution and abundance of the intermediate host snail and its schistosome parasites, thereby altering disease dynamics and transmission to humans [32].
The relationship between schistosomiasis and freshwater interaction has long been established as schistosomiasis is known to infect humans during water contact behaviours. This review showed that swimming, bathing, and exposure to river water were contributing factors [14]. Sick children excreted S. haematobium eggs in their urine while swimming and later produced furcocercariae that penetrated children’s skin exposed to the contaminated water. Similar findings were observed in a study conducted in Senegal, where variability and epidemiology of the disease were attributable to water-contact patterns [29].
Water-contact behaviour could be linked with occupation, socioeconomic and socio-cultural factors. A study by Ugbomoiko et al. reported that water contact is recreational and domestic [33]. The father’s occupation as a farmer was significantly associated with urinary schistosomiasis. Children participated in field activities with their fathers [24], demonstrating a lack of awareness among fathers about the risk of urinary schistosomiasis and failing to inform their children about its risk. As a result, the protective role of the family’s head of household being literate and knowledgeable about urinary schistosomiasis is critical in preventing transmission. Fishers and farmers have been exposed to such infestations because their jobs require frequent contact with unknown risk water, necessitating the immediate implementation of community-based schistosomiasis risk factor surveillance and targeted interventions.[25].
Out of 15 articles included in this review, the most common challenges are associated with a limited source of clean water [34]. Limited clean water sources place the community at a higher risk of infection with urinary schistosomiasis. The role of clean water in infectious diseases has always been an essential factor that has been highlighted globally. For example, in 2016, United Nations Children’s Fund (UNICEF 2016) developed a strategy for water, sanitation and hygiene (WASH) to achieve Sustainable Development Goal (SDG) 6 by 2030. One of the reasons for the formation of WASH was the strong association between poor WASH and neglected tropical diseases such as guinea worm, schistosomiasis, helminths, and trachoma that lead to undesired outcomes in the health of the children. Access to safe drinking water has been linked to a significant reduction in STH infection. A study in Côte d’Ivoire discovered that drinking tap water at home is associated with a lower risk of S. haematobium, hookworm and E. coli [35].
Apart from that, poor knowledge is also a barrier to controlling and eliminating USC. The baseline study revealed that the intensity of USC was high, corresponding with the lack of knowledge [36]. After two years, knowledge of urinary schistosomiasis had improved, from 56.6% to 93% of participants knowledgeable about urinary schistosomiasis, and the intensity of infection had decreased [16]. It was noted that the school children acquired information on schistosomiasis from the school and parents. Schools and parents play a significant role in preventing and controlling USC. Claude et al. [37] found that local children and adults in Gabon have a good understanding of urinary schistosomiasis, but 60% of the community practices risk-enhancing behaviour, notably in the area that lacks piped water. The issue shows that knowledge and proper water facilities must be in tandem to control and eliminate schistosomiasis.
Besides the limitation of clean water sources and poor knowledge, community practices are also found to be a challenge in the effort to control and eliminate urinary schistosomiasis. In the study conducted by Moyo et al. [11], it was found that tricky to prevent the community from visiting the infested sites for daily activities. Similar findings are also portrayed in the study conducted [37] involving 602 study participants. Out of the 602 study participants, 387(64%) participants reported urinating in a freshwater body and 152 (25%) participants regularly defecated in a freshwater body.
This review had limitations as most publications focused on assessing and treating primary school children. Other vulnerable populations, such as preschool children and children under six, may be at risk of underreporting. As non-English papers were not included in this review, language bias was possible. We overlooked findings from the grey literature because we limited our review to three databases and freely available, published, peer-reviewed full texts.
Several systematic reviews of USC have been conducted, but our review may be unique in that it focuses on recent meta-analyses of prevalence, risk factors in children, and challenges in preventing USC, while other papers may focus on other risk categories. Few studies, such as this one, highlight the difficulties in preventing and controlling the infection.
Conclusion and recommendations
Modifiable risk factors such as poor knowledge and practices need to address immediately. This could be achieved through continuous practical promotional activities by the relevant stakeholders such as the health care provider and school. It is crucial to ensure that intended messages are delivered to increase community awareness of urinary schistosomiasis.
In this review, USC remains a neglected tropical disease that needs further improvement despite various efforts implemented globally. The disparity in the incidence of urinary schistosomiasis between developed and underdeveloped countries is salient. It highlights those necessities, such as clean and adequate water supply, hinder the reduction of urinary schistosomiasis.
Given the negative impact of urinary schistosomiasis, a holistic approach involving the stakeholders such as parents, schools, and the government is needed to control and eliminate urinary schistosomiasis. Apart from that, a multisectoral partnership involving non-governmental organisations (NGOs) and the government is needed to ensure a clean and adequate water supply, as it has an essential role in reducing urinary schistosomiasis in the community.
Further research and development are needed, especially in underdeveloped countries. For example, a non-sewered sanitation system that uses nanomembrane technology could be helpful, especially in a limited water supply [38]. Besides that, policymakers should ensure adequate financing to build the appropriate infrastructure for the water supply.
Supporting information
S1 Checklist. Appendix.
Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist.
https://doi.org/10.1371/journal.pone.0285533.s001
(DOCX)
S1 Fig. Life cycle of Schistosoma haematobium in freshwater.
https://doi.org/10.1371/journal.pone.0285533.s002
(TIF)
S3 Fig. Meta-analysis on urinary schistosomiasis in children.
https://doi.org/10.1371/journal.pone.0285533.s004
(TIF)
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