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PLoS Negl Trop Dis
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PLOS Neglected Tropical Diseases
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10.1371/journal.pntd.0012462
PNTD-D-23-01653
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Schistosoma Mansoni
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Schistosomiasis
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Intestinal Schistosomiasis
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Schistosomiasis
Intestinal Schistosomiasis
Prevalence of human schistosomiasis in various regions of Tanzania Mainland and Zanzibar: A systematic review and meta-analysis of studies conducted for the past ten years (2013–2023)
Prevalence of human schistosomiasis in various regions of Tanzania Mainland and Zanzibar
https://orcid.org/0009-0001-0419-8697
Mbugi Nicolaus Omari Conceptualization Data curation Formal analysis Methodology Writing – original draft 1 2 *
Laizer Hudson Data curation Formal analysis Writing – review & editing 2 *
Chacha Musa Supervision Writing – review & editing 3 *
Mbega Ernest Supervision Writing – review & editing 1 *
1 The Nelson Mandela African Institution of Science and Technology, School of Life Sciences and Bioengineering, Arusha, Tanzania
2 Mbeya University of Science and Technology, College of Science and Technical Education, Mbeya, Tanzania
3 Arusha Technical College, Arusha, Tanzania
Ekpo Uwem Friday Editor
Federal University of Agriculture Abeokuta, NIGERIA
The authors have declared that no competing interests exist.

* E-mail: nicolausm@nm-aist.ac.tz (NOM); hudson.laizer@must.ac.tz (HL); musa.chacha@nm-aist.ac.tz (MC); ernest.mbega@nm-aist.ac.tz (EM)
9 9 2024
9 2024
18 9 e001246229 12 2023
17 8 2024
© 2024 Mbugi et al
2024
Mbugi et al
https://creativecommons.org/licenses/by/4.0/ 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.

Schistosomiasis is a significant public health problem in Tanzania, particularly for the people living in the marginalized settings. We have conducted a systematic review with meta-analysis on the prevalence of schistosomiasis to add knowledge towards the development of effective approaches to control the disease in Tanzania. Online databases namely, Pub Med, SCOPUS and AJOL, were systematically searched and a random effect model was used to calculate the pooled prevalence of the disease. Heterogeneity and the between studies variances were determined using Cochran (Q) and Higgins (I2) tests, respectively. A total of 55 articles met the inclusion criterion for this review and all have satisfactory quality scores. The pooled prevalence of the disease in Tanzania was 26.40%. Tanzania mainland had the highest schistosomiasis prevalence (28.89%) than Zanzibar (8.95%). Sub-group analyses based on the year of publication revealed the going up of the pooled prevalence, whereby for (2013–2018) and (2018–2023) the prevalence was 23.41% and 30.06%, respectively. The prevalence of the Schistosoma mansoni and Schistosoma hematobium were 37.91% and 8.86% respectively. Mara, Simuyu, and Mwanza were the most prevalent regions, with a pooled prevalence of 77.39%, 72.26%, and 51.19%, respectively. The pooled prevalence based on the diagnostic method was 64.11% for PCR and 56.46% for POC-CCA, which is relatively high compared to other tests. Cochrans and Higgins (I2) test has shown significant heterogeneity (p-value = 0.001 and I2 = 99.6). Factors including age, region, diagnostic method and sample size have shown significant contribution to the displayed heterogeneity. The pronounced and increasing prevalence of the disease suggests potential low coverage and possibly lack of involvement of some regions in the control of the disease. This, therefore, calls for an intensive implementation of control interventions in all endemic regions, preferably using an integrated approach that targets several stages of the disease lifecycle.

Author summary

Schistosomiasis is a devastating tropical and sub-tropical disease that disproportionately infects those in resource-limited settings, which causes death, morbidity and socioeconomic impact. The disease is caused by blood parasites under the genus Schistosoma. Tanzania is one of the schistosomiasis burdened countries in the sub-Saharan region. Praziquantel mass drug administration has been a predominant schistosomiasis control strategy in the country. We have conducted a systematic review and meta-analysis using a prevalence dataset from published literature, aiming at assessing the country’s schistosomiasis burden (prevalence) following several years of disease control. We further conducted a subgroup analysis to assess the contributing factors to the observed disease prevalence. The obtained information provides insight into the impact of schistosomiasis control in Tanzania, and highlights the potential for positive change and improvement in the country’s fight against this disease.

The author(s) received no specific funding for this work. PLOS Publication Stagevor-update-to-uncorrected-proof
Publication Update2024-09-19
Data AvailabilityData are provided as part of the submitted article (Table 1)
Data Availability

Data are provided as part of the submitted article (Table 1)
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pmc1. Introduction

Schistosomiasis is one of the most pervasive tropical and sub tropical neglected diseases caused by blood helminths that belong to the genus Schistosoma [1,2]. This genus comprises several species that infect a vast range of hosts; however, only six are of clinical importance, namely Schistosoma mansoni, Schistosoma japonicum, Schistosoma mekongi, Schistosoma guineansis, Schistosoma intercalatum and Schistosoma haematobium [3]. The first five species cause intestinal schistosomiasis, whereas the latter causes urogenital schistosomiasis. Schistosomiasis is of public health importance due to its socioeconomic impact, ranking second after Malaria [4]. Recent data shows that over 237 million people are infected by schistosomiasis on a global scale, consequently accounting for 280,000 mortalities yearly [5,6,7]. Of all continents, Africa particularly the Sub-Saharan region, is leading in terms of disease burden, carrying 90% of all global cases [6]. In the region, Tanzania marks the second country in terms of disease burden, only surpassed by Nigeria [8,9]. Typically, Schistosoma mansoni and Schistosoma hematobium causing intestinal and urogenital schistosomiasis respectively, are endemic species in Tanzania, which cumulatively contribute to the pronounced prevalence [10]. Tanzania is the union of two countries, Zanzibar and Tanganyika, which was later referred to as Tanzania mainland. These two parts of the country have different backgrounds regarding schistosomiasis control. In Zanzibar, the history of schistosomiasis control dates back to the 1980s, when the disease prevalence, particularly urogenital schistosomiasis, was high [11]. The control of the disease was enforced through praziquantel mass drug administration in schools. This initiative was further enhanced by the Zanzibar Elimination of Schistosomiasis Transmission (ZEST) project between 2011 and 2017 [12, 13]. During the project, biannual praziquantel mass drug administration was implemented in both Pemba and Unguja islands to schools and the community at large. In addition, over the course of the project, other control interventions including bio-control of snails and behavioural changes were also employed [12]. Since the inception of the mentioned control interventions, there has been a considerable decrease in the disease burden from above 50% to 5% in 2020 in both islands. In view of this, current control initiatives focus on the complete elimination of the disease to make Zanzibar amongst the few regions in sub-Saharan Africa to achieve interruption of disease transmission [11].

Meanwhile, schistosomiasis control in Tanzania’s mainland dates back to 2000s, when the Schistosomiasis and Soil-transmitted Helminths Control Programme (NSSCP) was founded [14]. NSSCP is a joint partnership between the Ministry of Health, Community Development, Gender, Elderly and Children (MoHCDGEC) and the Ministry of Education and Vocational Training (MoEVT) established with the support of the Schistosomiasis Control Initiative (SCI). The programme has done much on disease surveillance and control through mass drug administration (MDA) using praziquantel. The praziquantel MDA mainly focused on school children, and from 2009 to 2018, more than 33.3 million drugs were delivered to the mentioned group [15]. The program covers all administrative regions that are endemic to schistosomiasis (about 17 regions), with a particular focus on the regions in a northern-western zone, which are highly endemic to the disease [15, 16]. In the regions that have prevalence > 50, the program was further extended to other high-risk groups [16]. However, the disease prevalence is still very high across endemic areas in the country, ranging from 12.7% to 87.6% [14]. The disease is more abundant in societies living along the shoreline of Lake Victoria, particularly in the Mwanza region, with vulnerable groups being pre-school and school-aged children as well as women[5]. The vulnerability of the aforementioned groups is attributed to their routine domestic activities that potentially expose them to infected water [7].

Both forms of schistosomiasis (urogenital and intestinal) are acquired through skin penetration of infective larvae (cercariae) into susceptible hosts[4]. This occurs when a susceptible host is exposed to infected water, and hence, infective larvae penetrate and migrate to their resident sites, where they grow into adult worms [3,4]. In the host body, adult worms reside in various destinations specific to the schistosome species, where they copulate and lay eggs [3,4]. The laid eggs are responsible for the pathophysiology of the disease, which is then clinically manifested in two forms; the acute and chronic manifestations [3,4]. Summarily, clinical manifestations of urogenital schistosomiasis include dysuria, nutritional deficiencies, haematuria, hydronephrosis, urinary bladder squamous cell carcinoma, and urinary bladder lesions [5]. For intestinal schistosomiasis, medical conditions such as splenomegaly, hepatomegaly, and progressive periportal fibrosis are manifested [5].

Considering the WHO guideline, the control of schistosomiasis in Tanzania and elsewhere predominantly relied on preventive chemotherapy by using Praziquantel drug. However, there is a need to assess the impact of this control intervention on the disease burden over the years of its implementation. Therefore, the present systematic review compiles epidemiological data on the prevalence of schistosomiasis in both Tanzania mainland and Zanzibar from 2013 to 2023. This will provide baseline information regarding the country’s response to Praziquantel mass drug administration as the mainstay for disease control, as well as provide the highlights for potential improvements in the fight against schistosomiasis.

2. Methodology

2.1 Data acquisition

Computer-assisted searches in online databases including Pub Med, SCOPUS and AJOL were done by using advanced search options to obtain relevant articles. MeSH term options from PubMed were usedf to obtain some terminologies used in the material search. Whereby, the search term used were Schistosomiasis OR Bilharzia* OR Schistosoma* OR Katayama* AND Epidemiology OR Prevalence AND Tanzania OR Zanzibar in combination. The obtained articles were primarily screened based on the relevance of their titles and abstracts to the reviewed topic by applying the prior defined inclusion and exclusion criterion. Duplicates were also removed using Mendeley. Again, full screenings were further performed to obtain the final set of publications used to compose the present review article.

2.2 Exclusion and inclusion criteria

Publications excluded from the use in the present review include publications not written in the English language, titles not relevant to the reviewed topic, reporting prevalence dataset from countries other than Tanzania, duplicating results of the research work from large project or research group, non-human studies, containing pooled datasets from two countries or more, contain datasets from a prospective longitudinal study following mass drug administration, as well as articles assessing genetic dynamics among both S. hematobium and S. mansoni populations. Whereas published articles containing prevalence data from the Tanzanian population and not returning visitors from Tanzania collected within the past 10 years (2013 to 2023), reporting baseline data from the intervention studies, prevalence data of schistosomiasis in various regions of Tanzania mainland and Zanzibar, assessing sensitivity of various diagnostic techniques with a clearly defined sample size and number of cases were included.

2.3 Articles selection and data extraction

Following combining results from the searched online databases, author NM and HL scanned all retrieved publications based on the titles and abstracts for their eligibility to be fully reviewed. Eligible articles were full text reviewed by two independent authors (NM and HL) for their inclusion illegibility in data extraction. Articles from both authors that are matching were selected for data extraction. For the case of any mismatch other two authors (MC and EM) were consulted. Prior to data extraction, all duplicates were removed. Afterwards, data were independently abstracted by two authors (NM and HL) using a pre-designed form in Microsoft Excel. The form was pre-tested by all authors (NM, HL, MC, EM) prior to its use in data extraction. On the occasion that there was a difference in data extracted by the two authors from similar articles, other two authors were invited (MC and EM) to extract the data independently. Similar data extracted by at least three of the four authors was taken. Extracted data includes the author’s name, year of publication, study regions, diagnostic method used, sample size (study population), number of cases, target groups, study design used as well as the age range (Table 1).

2.4 Assessment of study quality and risk of bias

Quality and risk of bias for the selected publications were evaluated on the basis of criteria stipulated in the Joanna Briggs Institute critical appraisal checklist for use in reviews of prevalence studies[17]. Briefly, each criterion was accredited 1 grade if a criterion was met and 0 if a criterion was not met. Nine (9) was the maximum score given when all criteria were met, whereas 0 was the minimum score given to an article when none of the criteria were met. Articles scored cumulative grades ranging from 0–4 were regarded are of low quality, 5–7 moderate quality and 8–9 high quality. After that, articles demonstrating moderate to high quality were included in the present systematic review and meta-analysis. Authors (NM and HL) independently evaluated the quality of included publications.

2.5 Meta-analysis

Meta-analysis was done in line with the previously published protocol by employing a random effects model [17]. Through this, point estimates of the weighted prevalence of the datasets from the included studies were computed at 95% confidence intervals (CIs) and presented by forest plot. Heterogeneity, as well as variation between studies was assessed using Cochran’s Q (chi-square) and (Higgins) I2 tests, respectively. I2 values above 50% were considered to indicate substantial heterogeneity. For Cochran’s Q (chi-square) test, the heterogeneity was considered significant at p-value = 0.1. The univariate subgroup analysis to assess the contributing factors to the observed heterogeneity was computed with regard to the year of publication, region, diagnostic method, sample size, age of the participants and schistosoma species. The mentioned factors were grouped in the following order; year of publication into 2 groups; (2013–2018) and (2018–2023), regions into 17 groups; Ruvuma, Lindi, Mwanza, Dar es salaam, Morogoro, Mara, Simiyu, Shinyanga, Geita, Zanzibar, Kilimanjaro, Kagera, Dodoma and combination of regions such as (Kagera, Mara and Mwanza), (Mwanza and Shinyanga), (Mwanza and Kagera) and (Kagera, Mara, Shinyanga and Mwanza). Sample size was categorized into 3 categories; <100 (small), 100–499 (moderate) and >500 (large), age of the participant into 3 categories; <18, (18 and above) and all ages, schistostosoma species into 2 categories; S.mansoni and S. haematobium, and diagnostic method into 12 categories; Kato katz, PCR, POC-CCA, Mini FLOTAC, Sedimentation, Microscopy, Direct wet preparation, Urine filtration, Urine centrifugation, CAA, Direct smear and microhematuria. The factors demonstrating significant heterogeneity was subjected to multivariate subgroup analysis and the amount contributed by each factor or combination of significant factors (R2) was determined.

Additionally, publication bias was examined visually using a funnel plot and the degree of asymmetry was further confirmed by using Egger’s regression test. Whereby, it was assumed that the symmetrical distribution of the study effect sizes across the plot indicates the absence of the study bias. In contrast, the asymmetrical distribution reflects the presence of the study bias. All statistical analyses were done in R software version 4.3.0 using the meta prop function under the meta and metaphor package.

3 Results

3.1 Literature search results

3.1.1 Characteristics of the reviewed publications

A systematic literature search produced 1504 publications ranging from 2013 to 2023, from which only 55 met the inclusion criteria by reporting on the prevalence datasets from disparate regions of Tanzania and hence included in the present review work (Fig 1). Of the included publications, 3 reported prevalence datasets from women, 4 from preschool-aged children, 22 from school-aged children, 3 from both pre and school-aged children, 2 from both children and adults, 2 from children, 1 from HIV-infected children, 1 from psychiatric patients, 1 from adults with TB, 2 from adults with HIV, 1 from street children and orphans, 10 from adults, 3 from the general population, 1 from secondary school students and 1 from the university students (Table 1). On the other hand, the study design from the selected 55 publications was 44 cross-sectional studies, 1 case-control, 2 cohorts, 5 prospective longitudinal, 1 randomized controlled trial, and 2 study designs were not specified (Table 1).

10.1371/journal.pntd.0012462.g001 Fig 1 Conceptual framework of the literature search and screening process.

Among the selected publications, 30 assessed the prevalence of S. mansoni, 15 of S. hematobium, and 11 of both S. hematobium and S. mansoni. The regions from Tanzania were reported as follows; 1 publications report prevalence dataset from Ruvuma, 3 from Lindi, 3 from Mara, 23 from Mwanza, 5 from Dar es Salaam, 2 from Simiyu, 5 from Zanzibar, 2 from Shinyanga, 1 from Geita, 1 from Kagera, 4 from Morogoro, 2 from Dodoma and 1 from Kilimanjaro. Meanwhile, 2 publications report combined datasets from Kagera, Mara, Shinyanga and Mwanza, 1 from Mwanza and Shinyanga and 1 from Mwanza and Kagera (Table 1).

An array of diagnostic methods were used to screen both S. mansoni and S. hematobium whereby, Kato katz was the mostly used diagnostics method as reported by 30 studies, followed by urine filtration (n = 19), POC-CCA (n = 19), PCR (n = 5), microscopy (n = 4), urine concentration (n = 3), direct smear (n = 2), formal ether concentration (n = 3), CAA (n = 3), microhematuria (n = 1) and Mini FLOTAC (n = 2) (Table 1). The enrolled studies recruited a total of 122,674 individuals from Zanzibar as well as 12 regions of Tanzania mainland. The age of examined individuals ranges from 0 to 95 years.

10.1371/journal.pntd.0012462.t001 Table 1 General characteristics of the reviewed articles.

Author	Year of publication	Study area	Study design	Targeted species	Targeted group	Age (Years)	Diagnostic methods	Sample size	Cases	
Angelo et al.[18]	2018	Shinyanga	Longitudinal	S. hematobium	School-aged children	12 to 14	Urine filtration	282	98	
Bakuza et al.[19]	2018	Lindi	Cross-sectional	S. hematobium	Children	9 to 12	Urine filtration	190	44	
Barda et al.[20]	2013	Mwanza	Unspecified	S. mansoni	Children	4 to 19	Direct smear	201	8	
Barda et al. [20]	2013	Mwanza	Unspecified	S. mansoni	Children	4 to 19	Kato Katz	201	66	
Barda et al. [20]	2013	Mwanza	Unspecified	S. mansoni	Children	4 to 19	Mini FLOTAC	201	98	
Barda et al.[21]	2014	Mwanza	Cross-sectional	S. mansoni	School children and adults	Above 5	Mini FLOTAC	251	58	
Barda et al. [21]	2014	Mwanza	Cross-sectional	S. mansoni	School children and adults	Above 5	Formol ether concentration	251	32	
Barda et al. [21]	2014	Mwanza	Cross-sectional	S. mansoni	School children and adults	Above 5	Direct smear	251	9	
Barda et al. [21]	2014	Mwanza	Cross-sectional	S. mansoni	School children and adults	Above 5	Urine concentration	151	72	
Bukindu et al.[22]	2016	Mwanza	Cross-sectional	S. mansoni	School-aged children	8 to 18	Kato Katz	625	229	
Casacuberta et al. [23]	2016	Mwanza	Cross-sectional	S. mansoni	School-aged children	9 to 12	Kato Katz	404	303	
Casacuberta et al. [23]	2016	Mwanza	Cross-sectional	S. mansoni	School-aged children	9 to 12	POC-CCA	404	172	
Fanz et al. [24]	2023	Mwanza	Cross-sectional	S. mansoni	Orphans	6 to 18	POC-CCA	144	91	
Fanz et al. [24]	2023	Mwanza	Cross-sectional	S. mansoni	Street children	6 to 18	POC-CCA	122	103	
Fanz et al.[24]	2023	Mwanza	Cross-sectional	S. mansoni	Orphans	6 to 18	Kato Katz	144	28	
Fanz et al. [24]	2023	Mwanza	Cross-sectional	S. mansoni	Street children	6 to 18	Kato Katz	112	86	
Fulgence et al. [25]	2023	Dar es Salaam	Cross-sectional	S. mansoni	University students	19 to 33	Kato Katz	272	22	
Fuss et al.[26]	2018	Mwanza	Cross-sectional	S. mansoni	School-aged children	7 to 16	Kato Katz	297	253	
Fuss et al. [26]	2018	Mwanza	Cross-sectional	S. mansoni	School-aged children	7 to 16	POC-CCA	297	282	
Fuss et al. [26]	2018	Mwanza	Cross-sectional	S. mansoni	School-aged children	7 to 16	Real-time PCR	297	276	
Fuss et al.[27]	2020	Mwanza	Cross-sectional	S. mansoni	Adults	18 to 70	Kato Katz	36	12	
Fuss et al. [27]	2020	Mwanza	Cross-sectional	S. mansoni	Adults	18 to 70	POC-CCA	36	23	
Fuss et al. [27]	2020	Mwanza	Cross-sectional	S. mansoni	Adults	18 to 70	Serum real-time PCR	36	27	
Fuss et al. [27]	2020	Mwanza	Longitudinal	S. mansoni	Adults	18 to 70	Urine real-time PCR	36	11	
Fuss et al. [28]	2021	Mwanza	Cross-sectional	S. mansoni	Adults	17 to 70	POC-CCA	100	80	
Fuss et al. [28]	2021	Mwanza	Cross-sectional	S. mansoni	Adults	17 to 70	Serum real-time PCR	95	84	
Fuss et al. [28]	2021	Mwanza	Cross-sectional	S. mansoni	Adults	17 to 70	DBS real-time PCR	100	41	
Fuss et al.[28]	2021	Mwanza	Cross-sectional	S. mansoni	Adults	17 to 70	Kato Katz	98	43	
Kaatano et al. [29]	2015	Mwanza	Cross-sectional	S. mansoni	Adults	12 to 85	Kato Katz	388	121	
Kapiga et al. [30]	2021	Mwanza and Kagera	Cross-sectional	Schistosoma spp.	Adult	Above 18	CAA	1112	924	
Kayange et al.[31]	2020	Mwanza	Cross-sectional	S. mansoni	School-aged children	6 to 13	POC-CCA	507	253	
Kayange et al. [31]	2020	Mwanza	Cross-sectional	S. hematobium	School-aged children	6 to 13	Urine filtration	507	8	
Keller et al.[32]	2020	Zanzibar	Cross-sectional	S. hematobium	Children and adults	9 to 55	qPCR(Dra1 DNA)	792	212	
Keller et al. [32]	2020	Zanzibar	Cross-sectional	S. hematobium	Children and adults	9 to 55	Urine filtration	792	105	
Keller et al. [32]	2020	Zanzibar	Cross-sectional	S. hematobium	Children and adults	9 to 55	Microhaematuria	792	109	
Kinug’hi et al.[33]	2014	Mwanza	Cross-sectional	S. mansoni	Pre-school and school-aged children	3 to 13	Kato Katz	1,546	613	
Kinug’hi et al. [33]	2014	Mwanza	Cross-sectional	S. hematobium	Pre-school and school-aged children	3 to 13	Nucleopore filtration method	1,546	305	
Kinunghi et al.[34]	2017	Mara	Cross-sectional	S. mansoni	School-aged children	6 to 15	Kato Katz	928	794	
Kisiringyo et al. [35]	2020	Morogoro	Cross sectional	S. hematobium	School children	5 to 16	Formal-ether sedimentation	374	186	
Kisiringyo et al. [35]	2020	Morogoro	Cross sectional	S. mansoni	School children	5 to 16	Formal-ether sedimentation	374	1	
Knopp et al. [36]	2015	Zanzibar	Unspecified	S. hematobium	School-aged children	8 to12	Urine filtration	1740	58	
Knopp et al. [37]	2018	Zanzibar	Cross-sectional	S. hematobium	Adults	20 to 55	Urine filtration	18,155	490	
Knopp et al. [37]	2018	Zanzibar	Cross-sectional	S. hematobium	Children	9 to 12	Urine filtration	39,207	2,117	
Masikini et al. [38]	2019	Mwanza	Case-control	S. mansoni	HIV infected adults	Above 18	Microscopy	170	19	
Masikini et al. [38]	2019	Mwanza	Case-control	S. mansoni	HIV infected adults	Above 18	CAA	188	82	
Mazigo et al.[39]	2019	Mwanza	Cross-sectional	S. mansoni	HIV infected children	1 to 16	Kato Katz	103	11	
Mazigo et al. [39]	2019	Mwanza	Cross-sectional	S. mansoni	HIV infected children	1 to 16	POC-CCA	134	45	
Mazigo et al.[40]	2021	Mwanza	A prospective longitudinal	S. mansoni	School-aged children	7 to 17	Kato Katz	399	226	
Mazigo et al. [40]	2021	Mwanza	A prospective longitudinal	S. mansoni	School-aged children	7 to 17	POC-CCA	399	398	
Mazigo et al.[41]	2017	Mara	Cross-sectional	S. mansoni	Adults	18 to 89	Kato Katz	412	232	
Mazigo et al.[42]	2014	Mwanza	Cross-sectional	S. mansoni	Adults	21 to 55	Kato Katz	1,785	854	
Mazigo et al.[5]	2021	Ruvuma	Cross-sectional	S. hematobium	Pre and school-aged children	1 to 13	Urine filtration	1,560	13	
Mazigo et al. [5]	2021	Ruvuma	Cross-sectional	S. mansoni	Pre and school-aged children	1 to 13	Kato Katz	1,560	236	
Mazigo et al. [5]	2021	Ruvuma	Cross-sectional	S. mansoni	Pre and school-aged children	1 to 13	POC-CCA	574	125	
Mazigo et al. [43]	2018	Mwanza	Prospective longitudinal study	S. mansoni	General population	15 to 55	Kato Katz	419	242	
Mazigo et al. [43]	2018	Mwanza	Prospective longitudinal study	S. mansoni	General population	15 to 55	POC-CCA	419	365	
Mazigo et al.[44]	2018	Mwanza	Cross-sectional	S. mansoni	HIV infected adults	15 to 55	Kato Katz	979	463	
Mazigo et al. [44]	2018	Mwanza	Cross-sectional	S. mansoni	HIV infected adults	15 to 55	POC-CCA	979	592	
Mhimbira et al.[45]	2017	Dar es Salaam	Cohort	S. mansoni	Children and adults with TB	above 18	POC-CCA	597	55	
Mhimbira et al. [45]	2017	Dar es Salaam	Cohort	S. hematobium	Children and adults with TB	above 18	Urine filtration	597	19	
Mnkugwe et al.[46]	2020	Simiyu	Cross-sectional	S. hematobium	School-aged children	5 to 19	Kato Katz	830	752	
Mohamed et al. [47]	2018	Mwanza	Cross-sectional	S. mansoni	School-aged children	9 to 11	Kato Katz	327	103	
Mueller et al.[48]	2019	Mwanza	Cross-sectional	S. mansoni	General population	1 to 95	Kato Katz	930	641	
Mueller et al. [48]	2019	Mwanza	Cross-sectional	S. mansoni	General population	1 to 95	POC-CCA	930	879	
Mugono et al.[49]	2014	Mwanza	Cross-sectional	S. mansoni	School-aged children	4 to 15	Kato Katz	773	494	
Munisi et al.[50]	2016	Mara	Cross-sectional	S. mansoni	School-aged children	6 to 16	Kato Katz	513	431	
Mushi et al. [8]	2022	Lindi	Cross-sectional	S. hematobium	Preschool aged Children	under 5	Urine filtration	385	65	
Mushi et al. [51]	2022	Lindi	Cross-sectional	S. hematobium	School-aged children	6 to 17	Urine filtration	649	342	
Ndokeji et al.[52]	2016	Mwanza	Cross-sectional	S. mansoni	Pre-school and School-aged children	4 to 14	Kato Katz	454	363	
Ng’weng’weta et al. [53]	2017	Dar es Salaam	Cross-sectional	S. hematobium	Pre-school children	6 to 7	Urine centrifugation	424	8	
Ngasala et al. [54]	2019	Dodoma	Cross-sectional	S. hematobium	School-aged children	5 to 16	Microscopy	353	24	
Ngasala et al. [54]	2019	Zanzibar	Cross-sectional	S. hematobium	School-aged children	7 to 14	Microscopy	150	58	
Ngassa et al. [55]	2023	Kilimanjaro	Cross-sectional	S. hematobium	Women	15 to 45	Sedimentation	216	5	
Nkya [56]	2023	Morogoro	Cross sectional	S. hematobium	School children	6 to 16	Microscopy	884	287	
Nyundo et al.[57]	2017	Dodoma	Cross-sectional	S. mansoni	Psychiatric patients	12 to 69	Direct wet preparation and formol-ether concentration	233	12	
Ogweno et al. [58]	2023	Simiyu	Cross-sectional	S. mansoni	School-aged children	Unspecified	Kato Katz	363	150	
Palmeirim et al.[59]	2021	Morogoro	Cross-sectional	S. mansoni	School-aged children	6 to12	POC-CCA	427	53	
Pham et al. [60]	2023	Mwanza	Cross-sectional	Schistosoma spp.	Adults	Above 18	CAA	1,923	873	
Rite et al. [61]	2020	Geita	Cross-sectional	S. hematobium	Women	15 to 49	Urine filtration	426	19	
Rosinger et al.[62]	2018	Mwanza and Shinyanga	Cross-sectional	S. hematobium	Non-pregnant women	18 to 50	Urine filtration	209	12	
Rosinger et al. [62]	2018	Mwanza and Shinyanga	Cross-sectional	S. mansoni	Non-pregnant women	18 to 50	Kato Katz	205	11	
Ruganuza et al.[63]	2015	Mwanza	Cross-sectional	S. mansoni	Pre-school children	1 to 6	Kato Katz	400	178	
Ruganuza et al. [63]	2015	Mwanza	Cross-sectional	S. mansoni	Pre-school children	1 to 6	POC-CCA	400	320	
Said et al.[64]	2017	Dar es Salaam	Prospective longitudinal	Schistosoma spp.	Pre-school aged children	Under 5	POC-CCA	308	47	
Said et al. [64]	2017	Dar es Salaam	Prospective longitudinal	S. hematobium	Pre-school aged children	Under 5	Urine filtration	308	3	
Samweli et al. [65]	2023	Shinyanga	Cross-sectional	S. mansoni	Secondary school students	11 to 20	Kato Katz	620	12	
Shabani et al. [66]	2022	Kagera	Cross sectional	S. mansoni	Adults	18 to 55	Formal-ether sedimentation	328	36	
Sikalengo et al.[67]	2018	Dar es Salaam	Cohort study	S. mansoni	Adult TB patients	Above 18	Stool microscopy	460	8	
Sikalengo et al. [67]	2018	Dar es Salaam	Cohort study	S. mansoni	Adult TB patients	Above 18	POC-CCA	460	19	
Sikalengo et al. [67]	2018	Dar es Salaam	Cohort study	S. hematobium	Adult TB patients	Above 18	Urine filtration	460	16	
Sikalengo et al. [67]	2018	Morogoro	Cohort study	S. mansoni	Adult TB patients	Above 18	Stool microscopy	208	7	
Sikalengo et al. [67]	2018	Morogoro	Cohort study	S. mansoni	Adult TB patients	Above 18	POC-CCA	208	34	
Sikalengo et al. [67]	2018	Morogoro	Cohort study	S. hematobium	Adult TB patients	Above 18	Urine filtration	208	3	
Siza et al.[68]	2015	Kagera, Mara, Shinyanga and Mwanza	Cross-sectional	S. mansoni	School-aged children	7 to 16	Kato Katz	5,952	898	
Siza et al. [68]	2015	Kagera, Mara, Sinyanga and Mwanza	Cross-sectional	S. hematobium	School-aged children	7 to 16	Urine filtration	5,826	519	
Siza et al.[69]	2015	Kagera, Mara and Mwanza	Cross-sectional	S. mansoni	Adults	Not specified	Kato Katz	1,606	199	
Siza et al. [69]	2015	Kagera, Mara and Mwanza	Cross-sectional	S. mansoni	Adults	Not specified	Urine filtration	1,400	25	
Wang et al.[70]	2019	Zanzibar	A randomized controlled trial	S. hematobium	General population	Unspecified	Urine filtration	6,000	175	
Yangaza et al. [71]	2020	Dar es salaam	Cross sectional	S. hematobium	School children	7 to 15	Urine filtration	250	3	

3.2 Quality and risk of bias assessment

Examination of the study quality and risk of bias revealed the absence of low-quality studies; 23 publications had moderate quality hence scored (5–7), whereas 32 studies had high quality with score range of (8–9). The average score was 7.57, which indicates the overall moderate quality of the included publications. All studies used standard procedures of sample collection (stool, urine and blood) as well as valid diagnostic tests for the detection of both urogenital and intestinal schistosomiasis.

3.3 Pooled prevalence and sub-group analysis

Fifty-five (55) studies have reported on schistosomiasis prevalence datasets from various regions of Tanzania mainland and Zanzibar, which were used to estimate the country pooled prevalence. The pooled prevalence of schistosomiasis (both urogenital and intestinal) in Tanzania was 26.40% [95% CI: 20.73–32.98, I2 = 98.5%] (Fig 2). Cochran’s Q test portrayed substantial heterogeneity at p-value = 0.001, meanwhile, the between study variances determined using Higgins (I2) was also very high (99.6%).

10.1371/journal.pntd.0012462.g002 Fig 2 Forest plot showing the pooled prevalence of schistosomiasis in Tanzania.

Due to high heterogeneity, sub-group analyses were conducted to assess the effects of the contributing factors, which include Schistosoma species, year of publication, diagnostic methods, sample size, participant’s age as well as regions. Sub-group analysis based on the years of publication did not reveal significant heterogeneity at p-value = 0.2716, whereas other assessed factors such as diagnostic methods (p-value = < 0.0001), sample size (p-value = 0.0094), participant’s ages (p-value = < 0.0106), regions (p-value = 0.001) and schistosomes specie (p-value = < 0.0001) have shown significant contribution to the observed high heterogeneity. Furthermore, based on the years of publication, the sub-group analysis revealed the pooled prevalence of 23.41% [95% CI: 16.49–32.11] and 30.06% [95% CI: 21.97–39.61] at the following time intervals (2013–2018) and (2018–2023) respectively (Fig 3). Sub-group analysis based on the regions revealed the highest prevalence of schistosomiasis in Mara, Simiyu, and Mwanza with a prevalence of 77.39% [95% CI: 55.86–90.25, I2 = 98.5%], 72.26% [95% CI: 16.70–97.13, I2 = 99.6%], and 51.19% [95% CI: 44.79–57.56, I2 = 98.5%] respectively (Figs 4 and 5). Sub-group analysis of the prevalence dataset based on the Schistosoma species divulged the pooled prevalence of 8.86% [95% CI: 5.64–13.65, I2 = 99.5%] and 37.91% [95% CI: 31.05–45.29, I2 = 99.2%] for S. hematobium and S. mansoni respectively (Fig 6). Furthermore, sub-group analysis based on the diagnostic method showed the highest prevalence of PCR and POC-CCA with a pooled prevalence of 64.11 [95% CI: 31.89–87.21, I2 = 98.4%], 56.45 [95% CI 37.68–73.53, I2 = 99.1%] respectively (Fig 7 and 8). Estimated pooled prevalence based on the sample size sub group were 23.83 [95% CI: 15.59–34.64, I2 = 99.8%], 25.54 [95% CI: 19.38–32.87, I2 = 98.5%] and 0.5795 [95% CI: 0.3670–0.7660, I2 = 91.4%] for the sample size >500, 100–499 and <100 respectively (Fig 9). For the sub group analysis on the basis of the participant ages, the estimated prevalence of schistosomiasis were 29.47 [95% CI: 20.68–40.10, I2 = 99.7%], 15.19 [95% CI: 7.58–28.12, I2 = 99.6%] and 37.21 [95% CI: 27.24–48.40, I2 = 99.0%] for the following age groups; < 18, 18 and above and all ages respectively (Fig 10). The results of multivariate sub group analysis revealed that, factors including age (R2 = 100%), sample size (R2 = 100%), diagnostic method (R2 = 100%) and Region (R2 = 100%) contribute strongly to the overall heterogeneity (variability observed in the effect sizes) (p-value = 0.0001).

Since Zanzibar and Tanzania mainland have disparate histories regarding schistosomiasis control, additional sub group analysis were conducted to determine the estimated pooled prevalence of the mentioned areas. The estimated prevalence of schistosomiasis in Tanzania mainland was 28.89% [95% CI: 23.61–0.3482, I2 = 99.3%]; meanwhile, for Zanzibar was 8.95% [95% CI 5.11–15.22, I2 = 99.4%] (Fig 11).

10.1371/journal.pntd.0012462.g003 Fig 3 Forest plot showing the pooled prevalence of schistosomiasis in years of publication subgroups.

10.1371/journal.pntd.0012462.g004 Fig 4 Forest plot showing the pooled prevalence of schistosomiasis in region sub-group.

10.1371/journal.pntd.0012462.g005 Fig 5 Forest plot showing the pooled prevalence of schistosomiasis in region sub-group.

10.1371/journal.pntd.0012462.g006 Fig 6 Forest plot showing the pooled prevalence of schistosomiasis based on specie sub-group.

10.1371/journal.pntd.0012462.g007 Fig 7 Forest plot showing the pooled prevalence of schistosomiasis based on the diagnostic method.

10.1371/journal.pntd.0012462.g008 Fig 8 Forest plot showing the pooled prevalence of schistosomiasis based on the diagnostic method.

10.1371/journal.pntd.0012462.g009 Fig 9 Forest plot of the sub group analysis based on the sample size.

10.1371/journal.pntd.0012462.g010 Fig 10 Plot of the sub group analysis based on the participants ages.

10.1371/journal.pntd.0012462.g011 Fig 11 Forest plot showing the pooled prevalence of schistosomiasis in Tanzania mainland and Zanzibar.

3.4 Publication bias

Publication bias was assessed using a funnel plot of the effect sizes against standard error; as such, there was a symmetrical distribution of studies effect sizes along the plot, indicating the absence of the publication bias (Fig 12). However, egger’s regression analysis for funnel plot asymmetry outcome fails to confirm the absence of publication bias (p-value = 0.0099).

10.1371/journal.pntd.0012462.g012 Fig 12 Funnel plot showing the symmetrical distribution of studies along the plot.

4. Discussion

Schistosomiasis (both urogenital and intestinal) is an endemic disease in the Sub-Saharan region and the most devastating parasitic disease behind Malaria. Tanzania, being located in this region, is also highly affected by schistosomiasis. The present review assessed the prevalence of schistosomiasis in various regions of Tanzania mainland and Zanzibar and reported their pooled estimate values (prevalence). To the best of our knowledge, this is the first review reporting the prevalence of schistosomiasis in Tanzania for the past ten years (2013–2023).

The meta-analysis of the dataset from included studies revealed a high pooled prevalence of Schistosomiasis in Tanzania (26.40%). Notably, the prevalence was higher in Tanzania mainland than in Zanzibar. The lower prevalence in Zanzibar can be attributed to the successful implementation of the praziquantel mass drug administration strategy, which was carried out biannually for over 6 years [12,13]. Other strategies, such as behavioural changes and bio-control of the disease intermediate host, also contributed to the reduction of the disease burden [12,13]. However, the high prevalence in the mainland suggests that some regions may not have responded effectively to the control interventions or were not sufficiently involved in the treatment strategies, leading to the overall rise in prevalence.

The degree of heterogeneity and between study variances were high and attributed to factors including sample size, regions, diagnostic method, schistosoma species, and participant age. The prevalence of intestinal Schistosomiasis was high compared to urogenital schistosomiasis. The high prevalence of intestinal schistosomiasis can be attributed to the tendency of people to defecate near water bodies due to the presence of long vegetation and the availability of water for cleaning themselves, as was previously reported by Zacharia and coworkers (2020). This, therefore, fosters the spread of the disease through exposure of susceptible individuals to the infected water. The observed high prevalence of intestinal schistosomiasis is supported by the study done by Zacharia and coworkers (2020), which reported the re-infection rate and the prevalence of intestinal schistosomiasis at the global scale being higher relative to that of urogenital schistosomiasis [17]. The five-year interval analysis of schistosomiasis prevalence revealed a significant increase. As explained above, this surge may indicate inconsistency and lack of sustainability in the implementation of disease control interventions, as some regions might not have effectively responded to or have ceased implementing the treatment strategies, leading to a rise in overall prevalence. The north-western zone, which comprises regions including Mara, Simiyu, and Mwanza, has a pronounced pooled prevalence of the disease. The observed high prevalence could be affiliated with the presence of Lake Victoria, which is a potential source of transmission, especially when people conduct their socioeconomic activities such as fishing, agriculture, laundry, bathing, and mining, among others, thereby increasing the risk of subsequent re-infection [10].

On the other hand, proper and timely detection of schistosomiasis is an imperative step toward the efficient elimination of the disease. Failure to correctly diagnose the disease will, therefore, compromise the intensive work conducted to control the disease. Sub-group analysis based on the diagnostic methods divulged the high prevalence of schistosomiasis detected by PCR and POC-CCA. This indicates that the aforementioned methods are highly sensitive and, indeed, effective for the detection of both urogenital and intestinal schistosomiasis. As such, they should be widely adopted in the detection of schistosomiasis, as recommended by Bisetegn and coworkers, 2021 [72]. For sub group analysis on the basis of the participant age, it was revealed that participants of all ages were the most infected group. The high prevalence of this age group is because it encompasses all vulnerable groups, including school aged children, women of reproductive age, fishermen, etc., whose probability of exposure to infected water is relatively high. This observation agrees with another study that reported a high re-infection rate of schistosomiasis in individuals of all ages compared to other age groups [17]. Studies with small sample sizes had a high prevalence compared to those with moderate and large sample sizes. The reason behind the high prevalence of schistosomiasis in studies with small sample sizes could be the easy and intensive follow up compared to the ones with large sample sizes. Visual examination of the funnel plot portrayed the absence of the study bias as the study effect sizes were symmetrically distributed across the plot. However, eggers regression test outcomes failed to confirm the absence of the plot asymmetry; hence, it indicates the potential missing out of some studies, particularly the ones with small effect sizes.

5. Conclusion and recommendation

Despite extensive efforts put in place by the government of Tanzania in trying to eliminate schistosomiasis as a complement to the sustainable development goal number 3 of attaining health and wellbeing for all by 2030, the disease prevalence is still growing, as stipulated in this review. The regions surrounding Lake Victoria had the higher pooled prevalence and were considered the core hub for subsequent re-infection of schistosomiasis. The review also highlights that S. mansoni is the most prevalent species in Tanzania relative to S. hematobium. In view of that, an intensive deployment of praziquantel mass drug administration in combination with other control strategies in the endemic regions, particularly in the mainland part, is of paramount importance. The present study also proves that PCR and POC-CCA are the most sensitive methods for the detection of both urogenital as well as intestinal schistosomiasis as compared to the commonly used microscopy and direct smear methods. Given this, the aforementioned methods should be adopted during disease management interventions as the methods of choice for the identification of disease cases.

The authors acknowledge the management of the Nelson Mandela African Institution of Science and Technology for their administrative support, particularly by facilitating us with the office space, internet services, and other infrastructure needed during the whole process of writing this systematic review and meta-analysis.

10.1371/journal.pntd.0012462.r001
Decision Letter 0
Ekpo Uwem Friday Academic Editor
Tamarozzi Francesca Section Editor
© 2024 Ekpo, Tamarozzi
2024
Ekpo, Tamarozzi
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version0
8 Feb 2024

Dear Mr Mbugi,

Thank you very much for submitting your manuscript "Prevalence of Human Schistosomiasis in Various Regions of Tanzania Mainland and Zanzibar: A Systematic Review and Meta-Analysis of Studies Conducted for the Past Ten Years (2013-2023)" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. In light of the reviews (below this email), we would like to invite the resubmission of a significantly-revised version that takes into account the reviewers' comments.

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Sincerely,

Uwem Friday Ekpo, PhD

Academic Editor

PLOS Neglected Tropical Diseases

Francesca Tamarozzi

Section Editor

PLOS Neglected Tropical Diseases

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Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #1: Here, the authors present a review and meta-analysis of literature on prevalence of schistosomiasis across Tanzania. This is a valuable contribution to the literature however it requires a major revision to be worthy of publication. Overall there is a noticeable lack of proper citation. Either there are no citations used where there should be, or non-primary sources are used. There are also lots of grammatical errors. Finally, I think the authors are rather over egging the pudding when it comes to the importance of this work. As I have previously said, this is an important contribution, however there is an overuse of journalistic exaggeration that weakens the narrative.

My specific comments are below:

Make your code openly available.

- Species not specie.

- Please use line numbers to make reviewing easier.

- The final paragraph of the abstract, S. mansoni is not defined anywhere in the abstract prior to this. My initial thought is that the abstract is actually too long. Much of the detail could be exchanged for a more general overview because as it stands there are lots of details that without greater context do not necessarily make sense.

Introduction

- Schistosomiasis is not a pandemic. It is a tropical and sub-tropical disease that disproportionately infects those in resource limited settings. Even if we consider the small number of cases in Corsica, these were isolated, and transmission has died out.

- You say five species of clinical importance and then list six. Here, you can also use Schistosoma species name for the first one in the list and then S. species name for the following five.

- 5 (which should be 6) should be written out (five) as it is less than 10.

- What do you mean the “former 4” – they have not changed, I think you mean the first five cause intestinal disease?

- The mortality rates are not second after malaria. The socio-economic impact is second only to malaria. You have also not cited a primary source for this statement.

- Please use primary sources, again the article cited when stating that TZ is only surpassed by Nigeria for prevalence is not the primary source. The primary source is a 2009 piece by Hoetz et al. I should not have to go digging for primary sources and I would also suggest given the work of the SCI there are likely more up to date estimates available now.

- The statement “the country is endemic to…” is incorrect, it should be the other way around “S. mansoni and S. haematobium are endemic in Tanzania”.

- Adult worms do not contribute to morbidity. If someone has an entire single sex population, if there are no eggs there is no morbidity – as per the controlled human infections happening in the Netherlands.

I think section 2.3 should be data EXTRACTING not abstracting.

- “Meta-analysis was done in line with the previously published protocol by employing a random effects model.“ where is the citation for this if it is previously published? I believe Ayabina, Clark et al PLOS NTDS uses the same methodology but I am not sure whether this is the source here.

- Are meta and metaphor two separate packages? Citations please.

3.1 Characteristics of the reviewed publications

- I would like the citations for each of these descriptors. For example, the 3 papers that reported prevalence datasets from women, what are the citations for these? I wonder if a table would be a better way of presenting this information – though I think table 2 is too much. I would put these into your categories that you’re presenting in the first paragraph of this section.

- Same for the second paragraph, I wonder if you want to produce a map or something to summarise these locations. There is a tendency to focus epi research in the north of Tanzania, or on Zanzibar – I think a visual representation of this would be quite powerful.

Section 3.2

- What do you mean “several studies were pooled” – this is very woolly. Which studies? Why did you pool them? Be more explicit here.

- Take out “whereby,” it doesn’t make sense.

- What do you mean concurrently? This doesn’t make sense either.

- Your pooled time periods both include 2018, do your estimated prevalence both include 2018 also? This should not be this way. 2013-2017 and 2018-2023 or 2013-2018 and 2019-2023 should be used.

- What do you mean on the other hand? As opposed to what?

- In figure 1 why is there a dotted line just above 0.2? Is this the overall mean?

- What is the publication bias in comparison to? Spatially I am sure there is a bias.

Discussion

- “as regards to general disease sequelae” doesn’t make sense. – I would actually get rid of the first four lines of the discussion. There are no citations, it is repetitive of the introduction, and it is poorly written. Focus on the findings, rather than trying to make an unsubstantiated point to make the work seem more important.

- The second paragraph of the discussion lacks direction – what is the point that the authors are trying to make?

- Stop using journalist language like “alarming” – just report on what you have and put it into the context of the literature without fear mongering.

- “The high prevalence observed indicates that the rate of reinfection is still very high despite the implementation of several rounds of disease control interventions” There is no description of the intervention programmes underway in TZ, nor any citations to support this statement. If the authors want to make the point that treatment programmes aren’t working (which I have no doubt they aren’t based on results from other SSA countries) then there needs to be a more description of the activities that are in place.

- “As a consequence, there is alarming potential existence of a resistant strain of S. mansoni circulation amongst our population.” The work you mention (but do not properly cite) is not evidence for resistance. There is very little evidence to support PZQ resistance (see work by D. Berger, C. Faust and others).

- “This warrants the use of new and most effective strategies preferably the multifaceted approach” – what are the most effective strategies? What is THE multifaceted approach? There are no citations here and no concrete examples of what these interventions should be. I feel like the “conclusions” part would actually make a good opening to your discussion.

- Your review provides ZERO evidence of treatment resistance, this is a dangerous message to spread when there is so little evidence to support this hypothesis in the first place. In reality, there are so few people treated in the grand scheme of transmission, that the refuge population of worms is probably larger than those exposed to treatment, such that the selective pressure to generate resistance just is not there.

- I don’t understand why there is a section 5. Surely the normal format is that the discussion contains conclusions and recommendations.

- I fundamentally disagree that POC-CCA is the best for urogenital infection (for example https://doi.org/10.1179/136485908X337490)

Reviewer #2: I have presented my comments in the attached document.

--------------------

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Reviewer #2: No

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Attachment Submitted filename: Comments.docx

10.1371/journal.pntd.0012462.r002
Author response to Decision Letter 0
Submission Version1
23 Mar 2024

Attachment Submitted filename: Author response to reviewers comments.docx

10.1371/journal.pntd.0012462.r003
Decision Letter 1
Ekpo Uwem Friday Academic Editor
Tamarozzi Francesca Section Editor
© 2024 Ekpo, Tamarozzi
2024
Ekpo, Tamarozzi
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version1
20 Apr 2024

Dear Mr Mbugi,

Thank you very much for submitting your manuscript "Prevalence of Human Schistosomiasis in Various Regions of Tanzania Mainland and Zanzibar: A Systematic Review and Meta-Analysis of Studies Conducted for the Past Ten Years (2013-2023)" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. The reviewers appreciated the attention to an important topic. Based on the reviews, we are likely to accept this manuscript for publication, providing that you thoroughly modify the manuscript according to all the review recommendations. Please do taje oarticular care in shortening the text, as required, and avoid overinterpretation of results or misleading conclusions.

Please prepare and submit your revised manuscript within 30 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email.

When you are ready to resubmit, please upload the following:

[1] A letter containing a detailed list of your responses to all review comments, and a description of the changes you have made in the manuscript.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Thank you again for your submission to our journal. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Uwem Friday Ekpo, PhD

Academic Editor

PLOS Neglected Tropical Diseases

Francesca Tamarozzi

Section Editor

PLOS Neglected Tropical Diseases

***********************

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #1: (No Response)

Reviewer #2: (No Response)

--------------------

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #1: - The abstract is way too long and contains unnecessary information. At most I would expect an abstract to be ~300 words. You have four paragraphs. That is not an overview that is just your methods copied and pasted. For example:

- Remove “The prevalence datasets from the included studies were analyzed by using R software version 4.3.0”

- Remove “via meta prop function under the meta and metafor package”

Lines 42-43: What do you mean a time-dependent increase? You just mean it is going up? Do not try to sound fancy, just tell me what your data show. And how does that show an increasing rate of reinfection specifically? Surely it shows an increase in the force of infection?

Line 45: Species.

Line 47: I said this last time you submitted this article and I say it again. There is practically no evidence to support the statement that there is emerging treatment resistance in S. mansoni. Remove this statement. It is not helpful to management programmes and is fundamentally untrue. Consider the ecology and evolution of S. mansoni – there is a massive refugia because so many people are untreated and because there are so many thousands of cercaria produced. The selective pressure to force resistance into fixation in a population is just not there. Genomic evidence supports this. Stop using this trope. This goes for its mention in the discussion too.

Is it not the case that Tanzania has stopped the schistosomiasis programme now? Perhaps this deserves a mention in the introduction as I fear it is a massive mistake.

Line 239: Remove “generally” – you have reported the exact number of participants across all studies. There is nothing general about that.

Table 1 - Personally, I would put this table in the supplementary material.

I am interested to know more about your “quality” assessment. Personally, I think there is a tendency for poor statistics in schistosomiasis research and I would like to know if this was a metric in your assessment.

Line 255 remove “using the metaprop function” this does not really mean anything to someone unfamiliar with the package and should be in your methods not your results.

Lines 264 – theres no such thing as a p value of 0.

Line 342 – I am still confused by your use of “high rates of reinfection” – it is the force of infection that is high surely. And if you are claiming that treatment is not working because of resistance, then people are not getting reinfected, they are still infected. Whilst I can imagine that reinfection rates are high in areas like Mwanza where contact with contaminated water is constant, I do not agree that overall your results show high rates of reinfection.

340 to 366 – this paragraph is enormous and meandering. What is your point?

Lines 354 – 356 – I have no idea what point you are trying to make here.

Line 375 you say “participants of all ages” then go on in the following to say “this age group”. What age group, you have just said all age groups.

I feel like your discussion just repeats a lot of your results. This makes your discussion incredibly repetitive and long and quite boring to read. I would like to see how your results are fitting in with the wider literature and what this all means for control.

Reviewer #2: (No Response)

--------------------

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Reviewer #2: No

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References

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article's retracted status in the References list and also include a citation and full reference for the retraction notice.

Attachment Submitted filename: Comments.docx

10.1371/journal.pntd.0012462.r004
Author response to Decision Letter 1
Submission Version2
2 May 2024

Attachment Submitted filename: Author response to reviewers comments.docx

10.1371/journal.pntd.0012462.r005
Decision Letter 2
Chai jong-Yil Section Editor
Ekpo Uwem Friday Academic Editor
© 2024 Chai, Ekpo
2024
Chai, Ekpo
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version2
5 Jul 2024

Dear Mr Mbugi,

Thank you very much for submitting your manuscript "Prevalence of Human Schistosomiasis in Various Regions of Tanzania Mainland and Zanzibar: A Systematic Review and Meta-Analysis of Studies Conducted for the Past Ten Years (2013-2023)" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. The reviewers appreciated the attention to an important topic. Based on the reviews, we are likely to accept this manuscript for publication, providing that you modify the manuscript according to the review recommendations.

Please prepare and submit your revised manuscript within 30 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email.

When you are ready to resubmit, please upload the following:

[1] A letter containing a detailed list of your responses to all review comments, and a description of the changes you have made in the manuscript.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Thank you again for your submission to our journal. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Uwem Friday Ekpo, PhD

Academic Editor

PLOS Neglected Tropical Diseases

jong-Yil Chai

Section Editor

PLOS Neglected Tropical Diseases

***********************

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #2: (No Response)

Reviewer #3: The methods were carried out in line with a systematic review and were very informative and easy to follow. The fact that most authors were included in the review process is excellent in avoiding subjective choices.

I have some minor comments for the methods:

In the exclusion and inclusion criteria I would like to have understood the justification for two points:

• Not including studies which included data sets from longitudinal studies following mass drug administration - what is the reason for this? Could you not have included any baseline data from these studies?

• Studies assessing genetic dynamics among S. haematobium populations – again can you explain why this is. Furthermore, I would like to remind the authors that to avoid reviewer bias all inclusion and exclusion criteria should be set before any reviewing takes place, therefore surely this exclusion criteria should include all species of Schistosoma unless there is a specific reason why S. haematobium should be excluded and others not.

Can the authors explain why they chose to subgroup the publication years as they did, is there specific justification for splitting them into a five-year period? Was the number of studies too low to be include each year separately?

Finally, can the authors explain how they ensured that articles were not using the same datasets, it is not uncommon for a lab group to use the same dataset with different focus but both reporting prevalence. Please can the authors state how they ensured they were not duplicating data here. And add this to the exclusion criteria.

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #2: (No Response)

Reviewer #3: Table 1 – Can this table be ordered by either author name (alphabetically) or year or sample size? This would make it easier to read.

I was surprised to not see any articles with first author of either Pennance or Trippler in this table as they have both carried out extensive work in Zanzibar, but perhaps this is due to the reason above – that they are using datasets from previous studies by Knopp et al. If this was made clear in the exclusion criteria it would not be so surprising that the articles by these authors are not in the table. Otherwise, can the authors check that articles by these authors should not have been included.

In the subgroup analysis it would have been informative to see prevalence stratified by region and parasite together so we can really see what is happening in each region. As some regions have very low eg S. mansoni and very high S. haematobium the pooled prevalence would not be very informative as will be in the middle of the two.

The forest plots are well laid out and easy to read.

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #2: (No Response)

Reviewer #3: Line 346 states that the high prevalence of S. mansoni prevalence can be attributed to the tendency of people to defecate near water bodies – where in this review did the authors find this? If this was from other studies, please be clear of this.

Line 352 – the authors should be careful with what they say their results show – an increase of pooled prevalence from all parasite species over all regions does not necessarily show an inefficiency of PZQ by MDA as a disease control and elimination strategy. As this is pooled prevalence, it could be that some regions have responded very well to MDA, but this is diluted by other regions which either had not been involved in treatment strategies or had low coverage due to unknown reasons – but we cannot know this from the data presented here. Furthermore, some regions will have had additional control strategies such as snail control etc. but this is not accounted for in the results. The authors themselves state that the control interventions initiated by ZEST in the islands has reduced disease burden from above 50% to below 5%, therefore contradicting the aforementioned claim that control interventions are not working in the country.

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #2: (No Response)

Reviewer #3: (No Response)

--------------------

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #2: The authors have addressed the comments raised in my previous review report, and I see significant improvement. However, before being accepted, I recommend that the manuscript be revised by a professional English language editor.

Reviewer #3: The introduction was particularly interesting and covered the history of control strategies in the country well. I felt very informed and ready to read the rest of the article by the end of the introduction.

One comment for the intro:

Line 73 – High prevalence does not necessarily mean high morbidity, the authors say Tanzania marks the second country in terms of high disease morbidity rate, however neither reference cited here support this claim. Reference 6 states that there is significant morbidity in Tanzania, but they cite a different study to support this and do not report any morbidity results themselves. Reference 68 does not specifically talk about morbidity in Tanzania.

Overall summary:

My only real issue with this article is that I do not agree with the authors claim of what it shows the results can be used for. Line 128 they state that the results from this article can be used as a baseline roadmap for the proper allocation of resources and in the discussion line 333 they state that the observed prevalence indicates that the force of infection is still very high. I find it difficult to see how pooled prevalence of ten years tells us anything about what is happening at the moment, or can be used as a roadmap to inform future strategies. I can see how the data contained in this article could be very useful in informing control strategies if they had looked at how prevalence had changed in response to control strategies over the years. But a pooled prevalence from many different years and regions and parasite species does not allow us to inform on the current situation. Reporting of this pooled prevalence is interesting but does not inform in the way the authors state it does.

In conclusion, this is a well written and well carried out systematic review of the prevalence of Schistosoma over a ten-year period. However, I think some of the claims made by the authors of what these data can actually show are not founded in the way the results are presented.

--------------------

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Reviewer #2: No

Reviewer #3: No

Figure Files:

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org.

Data Requirements:

Please note that, as a condition of publication, PLOS' data policy requires that you make available all data used to draw the conclusions outlined in your manuscript. Data must be deposited in an appropriate repository, included within the body of the manuscript, or uploaded as supporting information. This includes all numerical values that were used to generate graphs, histograms etc.. For an example see here: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001908#s5.

Reproducibility:

To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option to publish peer-reviewed clinical study protocols. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

References

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article's retracted status in the References list and also include a citation and full reference for the retraction notice.

10.1371/journal.pntd.0012462.r006
Author response to Decision Letter 2
Submission Version3
16 Jul 2024

Attachment Submitted filename: Author response to reviewers comments (a).docx

10.1371/journal.pntd.0012462.r007
Decision Letter 3
Chai jong-Yil Section Editor
Ekpo Uwem Friday Academic Editor
© 2024 Chai, Ekpo
2024
Chai, Ekpo
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version3
17 Aug 2024

Dear Mr Mbugi,

We are pleased to inform you that your manuscript 'Prevalence of Human Schistosomiasis in Various Regions of Tanzania Mainland and Zanzibar: A Systematic Review and Meta-Analysis of Studies Conducted for the Past Ten Years (2013-2023)' has been provisionally accepted for publication in PLOS Neglected Tropical Diseases.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

Should you, your institution's press office or the journal office choose to press release your paper, you will automatically be opted out of early publication. We ask that you notify us now if you or your institution is planning to press release the article. All press must be co-ordinated with PLOS.

Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Uwem Friday Ekpo, PhD

Academic Editor

PLOS Neglected Tropical Diseases

Jong-Yil Chai

Section Editor

PLOS Neglected Tropical Diseases

***********************************************************

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #3: Yes

**********

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #3: Yes

**********

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #3: Yes

**********

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #3: None

**********

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #3: I think this is a very interesting and well presented research article. Thank you for answering my previous questions and actioning my suggestions. I was a little disappointed that my suggestion to see a sub group analysis of species and region together was not actioned. I do think this would be a more informative way to understand the pooled prevalence in each region (stratified by species), and I would have been interested to see these results. However, as this is one point and is not imperative to the article results, and the overall paper is very good, I decided not to push it and to accept the article as it is. Thank you for spending the time doing this meta-analysis, it is very obvious you have put in a huge amount of work into this.

**********

PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #3: No

10.1371/journal.pntd.0012462.r008
Acceptance letter
Chai jong-Yil Section Editor
Ekpo Uwem Friday Academic Editor
© 2024 Chai, Ekpo
2024
Chai, Ekpo
https://creativecommons.org/licenses/by/4.0/ 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.
25 Aug 2024

Dear Mr Mbugi,

We are delighted to inform you that your manuscript, "Prevalence of Human Schistosomiasis in Various Regions of Tanzania Mainland and Zanzibar: A Systematic Review and Meta-Analysis of Studies Conducted for the Past Ten Years (2013-2023)," has been formally accepted for publication in PLOS Neglected Tropical Diseases.

We have now passed your article onto the PLOS Production Department who will complete the rest of the publication process. All authors will receive a confirmation email upon publication.

The corresponding author will soon be receiving a typeset proof for review, to ensure errors have not been introduced during production. Please review the PDF proof of your manuscript carefully, as this is the last chance to correct any scientific or type-setting errors. Please note that major changes, or those which affect the scientific understanding of the work, will likely cause delays to the publication date of your manuscript. Note: Proofs for Front Matter articles (Editorial, Viewpoint, Symposium, Review, etc...) are generated on a different schedule and may not be made available as quickly.

Soon after your final files are uploaded, the early version of your manuscript will be published online unless you opted out of this process. The date of the early version will be your article's publication date. The final article will be published to the same URL, and all versions of the paper will be accessible to readers.

Thank you again for supporting open-access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Shaden Kamhawi

co-Editor-in-Chief

PLOS Neglected Tropical Diseases

Paul Brindley

co-Editor-in-Chief

PLOS Neglected Tropical Diseases
==== Refs
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2 Walker A. Insights into the functional biology of schistosomes. Parasites and Vectors. 2011;4 (1 ):2–7. doi: 10.1186/1756-3305-4-203 21210995
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9 Mazigo HD , Nuwaha F , Kinung’hi SM , Morona D , de Moira AP , Wilson S , Heukelbach J , Dunne DW . Epidemiology and control of human schistosomiasis in Tanzania. Parasites & vectors. 2012;5 :1–20. doi: 10.1186/1756-3305-5-274 22212459
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12 Knopp S , Mohammed KA , Ali SM , Khamis IS , Ame SM , Albonico M , Gouvras A , Fenwick A , Savioli L , Colley DG , Utzinger J . Study and implementation of urogenital schistosomiasis elimination in Zanzibar (Unguja and Pemba islands) using an integrated multidisciplinary approach. BMC Public Health. 2012; 12 :1–3.22214479
13 Knopp S , Person B , Ame SM , Mohammed KA , Ali SM , Khamis IS , Rabone M , Allan F , Gouvras A , Blair L , Fenwick A . Elimination of schistosomiasis transmission in Zanzibar: baseline findings before the onset of a randomized intervention trial. PLoS neglected tropical diseases. 2013; 7 (10 ):e2474. doi: 10.1371/journal.pntd.0002474 24147165
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16 Chaula SA , Tarimo DS . Impact of praziquantel mass drug administration campaign on prevalence and intensity of Schistosoma haemamtobium among schoolchildren in Bahi district, Tanzania. Tanzania journal of health research. 2014; 16 (1 ). doi: 10.4314/thrb.v16i1.1 26867266
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23 Casacuberta M , Kinunghi S , Vennervald BJ , Olsen A . Evaluation and optimization of the Circulating Cathodic Antigen (POC-CCA) cassette test for detecting Schistosoma mansoni infection by using image analysis in school children in Mwanza. PAREPI. 2016;1 (2 ):105–15. Available from: 10.1016/j.parepi.2016.04.002.
24 Franz A , Fuss A , Mazigo HD , Ruganuza D , Müller A . Prevalence of Schistosoma mansoni, soil-transmitted helminths and intestinal protozoa in orphans and street children in Mwanza city, Northern Tanzania. Infection. 2023;51 (5 ):1399–406. Available from: doi: 10.1007/s15010-023-01999-9 36805439
25 Fulgence M , Mustafa U-K , Bakuza JS . Prevalence and Burden of Gastrointestinal Parasites among University Students at Dar es Salaam University College of Education, Tanzania. Tanzania J Sci. 2023;49 (2 ):369–78.
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