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PLOS Neglected Tropical Diseases logoLink to PLOS Neglected Tropical Diseases
. 2022 Jun 30;16(6):e0010458. doi: 10.1371/journal.pntd.0010458

Mapping of schistosomiasis and soil-transmitted helminthiases across 15 provinces of Angola

Elsa Palma Mendes 1, Hajra Okhai 2, Rilda Epifânia Cristóvão 1, Maria Cecília Almeida 1, Nzuzi Katondi 3, Ricardo Thompson 4, Sylvain Mupoyi 4, Pauline Mwinzi 4, Onesime Ndayishimiye 5, Ferdinand Djerandouba 5, Mary Chimbilli 5, Julio Ramirez 5, Erna Van Goor 5, Sergio Lopes 5,*
Editor: Christine M Budke6
PMCID: PMC9278740  PMID: 35771862

Abstract

Introduction

Schistosomiasis (SCH) and soil transmitted helminthiases (STH) have been historically recognized as a major public health problem in Angola. However, lack of reliable, country wide prevalence data on these diseases has been a major hurdle to plan and implement programme actions to target these diseases. This study aimed to characterize SCH and STH prevalence and distribution in Angola.

Methods

A country wide mapping was conducted in October 2018 (1 province) and from July to December 2019 (14 provinces) in school aged (SAC) children in 15 (of 18) provinces in Angola, using WHO protocols and procedures. A total of 640 schools and an average of 50 students per school (N = 31,938 children) were sampled. Stool and urine samples were collected and processed using the Kato-Katz method and Urine Filtration. Prevalence estimates for SCH and STH infections were calculated for each province and district with 95% confidence intervals. Factors associated with SCH and STH infection, respectively, were explored using multivariable logistic regression accounting for clustering by school.

Results

Of the 131 districts surveyed, 112 (85.5%) are endemic for STH, 30 (22.9%) have a prevalence above 50%, 24 (18.3%) are at moderate risk (prevalence 20%-50%), and 58 (44.3%) are at low risk (<20% prevalence); similarly, 118 (90,1%) of surveyed districts are endemic for any SCH, 2 (1.5%) are at high risk (>50% prevalence), 59 (45.0%) are at moderate risk (10%-50% prevalence), and 57 (43.5%) are at low risk (<10% prevalence). There were higher STH infection rates in the northern provinces of Malanje and Lunda Norte, and higher SCH infection rates in the southern provinces of Benguela and Huila.

Conclusions

This mapping exercise provides essential information to Ministry of Health in Angola to accurately plan and implement SCH and STH control activities in the upcoming years. Data also provides a useful baseline contribution for Angola to track its progress towards the 2030 NTD roadmap targets set by WHO.

Author summary

Neglected Tropical Diseases (NTD) still affect nearly 1 billion people worldwide and are a major public health problem in Angola. Schistosomiasis (SCH) and soil transmitted Helminthiases (STH) affect disproportionally school aged children (SAC). In endemic areas, implementation of preventive chemoprevention through school-based Mass Drug Administration Campaigns is a key strategy used to reduce the burden of these infections. Mapping of schistosomiasis and soil transmitted helminthiases is essential to know where transmission occurs and is used to inform interventions planning. A country wide SCH and STH mapping was conducted across 15 of the 18 provinces of Angola. Parasitological analysis of nearly 32,000 children was conducted to detect SCH and STH infections and determine the prevalence of these diseases. Eighty Six percent of the mapped districts are endemic for STH and 22.9% have a prevalence above 50%. Similarly, 90% of surveyed districts are endemic for SCH. There were higher STH infection rates in the northern provinces of Malanje and Lunda Norte, and higher SCH infection rates in the southern provinces of Benguela and Huila. These results are of vital importance to map the prevalence of SCH and STH in Angola and to plan adequate interventions that support NTD control across the country.

Introduction

Neglected Tropical Diseases (NTD) are a group of poverty-related diseases, which are often chronic conditions impact nearly 1 billion an individual’s social and economic contributions worldwide [1]. Soil-transmitted helminthiases (STH) and schistosomiasis (SCH) can be controlled through interventions including preventive chemotherapy (often carried out as mass drug administration (MDA)) with impact and reinfection dependant on several factors such as the frequency, delivery and coverage of the campaigns, water and sanitation conditions, water contact patterns and sociodemographic factors [26].

Since the 2012 London Declaration on NTD, a global effort to eliminate NTDs was set and now reinforced with World Health Organization’s (WHO) road map for neglected tropical diseases 2021–2030 [1]. Regular treatment, adequate monitoring and evaluation are deemed as critical to achieve 2030 targets. In this context, mapping of SCH and STH is essential to know where transmission occurs and inform targeted interventions [7].

In Angola, STH and SCH are a recognized public health problem [8], with approximately 5–10% of the population in need of preventive chemotherapy for both diseases [1]. There is little published information on the distribution of these diseases and existing data are either outdated or covering limited geographical areas [9,10]. Passive data collection carried out in the mid 1900’s showed increasing Schistosoma haematobium cases reported in a number of provinces [11,12] and a survey in Bié confirmed that more than half of the population had urogenital SCH [13]. Subsequent surveys confirmed the existence of high prevalence rates of S. haematobium in both Malange [14] and in Huila provinces [1517]. Additional mapping work carried out in Benguela, and Luanda found 93% of SAC to be infected with S. haematobium [18]. From 1980’s to 2000, the burden of SCH in Angola has been solely based on these estimations [1921].

In contrast, for STH, surveys carried out in the 1950s in Zaire, Malange and Benguela estimated that up to 90% of the population was infected with Hookworm [11,14]. In Cuando Cubango, Huila and Kwanza Norte provinces, STH prevalence ranged from 65%-96% with Hookworm prevalence ranging from 40%-85% [15,22,23]. The first STH nationwide mapping conducted in 1964 registering prevalence around 75% in provinces like Huambo, Uige and Zaire [24]. Later surveys carried out in Bie found 86% of children had co-infections of 2 or more helminths [25]. While these referenced studies have shown a the presence of SCH and STH across Angola, their size and scope could not provide reliable prevalence estimates at district level, highlighting the need to conduct a country wide mapping.

In 2005, a STH and SCH mapping was carried out by the Angolan Ministry of Health (MoH) supported by the United Nations Children’s Fund (UNICEF) and WHO based on ecological regions. Results showed estimated nationwide urogenital SCH prevalence in Angola was 28%, with higher incidence in the southern (40,6%), central plateau (39,6%) and northern provinces [26]. STH was reported at 40% prevalence across the country with Ascaris (25,0%) and Hookworm (9,8%) reported as dominant [26]. Data from northern and central Angola confirms the pattern of predominance of Ascaris in SAC but also highlights the burden of Trichuris infection [9,27,28].

In 2014, a baseline mapping of SCH and STH infections was conducted through a collaboration between the Angolan Ministry of Health (MoH) The MENTOR Initiative (MENTOR) and the End Fund in the provinces of Uige, Zaire and Huambo. The mapping measures SCH and STH prevalence at district level as recommended by WHO confirming the high burden of STH, particularly in Uige but also moderate prevalence of SCH infections (from 10%-15%) with significant variations between districts within each province [29].

Since 2014, preventive chemotherapy interventions have been implemented firstly in Huambo, Uige and Zaire provinces followed by Cuanza Sul, Bié and Cuando Cubango in 2017, and Bengo in 2019. Recognizing the need to arrange intervention based on reliable mapping data, the MoH, supported by World Health Organization, led a country wide SCH and STH mapping exercise in October 2018 (1 province) and from July to December 2019 (14 provinces). The objective of this study was to quantify the prevalence and distribution of these diseases across fifteen provinces in Angola in order to be able to adequately plan preventive chemotherapy interventions. A secondary aim of this project was to explore whether the presence of a latrine or water source in the school reduced the risk of infection.

Methods

Ethics statement

This mapping was approved by the Angola Ministry of Health Ethics Committee (Approval number 27/2018) in June 2018. Informed Consent was sought from participants parents. The team liaised with School directors prior to the survey to ensure parents were aware of the benefits and harms of participating in the survey. Parents were provided with an explanatory information sheet and a consent form to take home to decide. Parents were asked to send their children to school with the signed form if they agreed.

All students participated in the mapping voluntarily. Children were briefed on the objectives of the mapping and only took part if they verbally assented to participate.

All data was kept anonymous. No personal information was collected as children were identified through a unique identifier number. All children enrolled were treated with a dose of Albendazole and Praziquantel according to their height.

Study design

A cross sectional survey using the standard WHO method for mapping [30] was implemented in October 2018 (Bengo province). Thereafter, from July to December 2019 in the remaining fourteen Angolan provinces not yet mapped for STH and SCH (Benguela, Bié, Cabinda, Cunene, Cuando Cubango, Cuanza Norte, Cuanza Sul, Lunda Norte, Lunda Sul, Malanje, Moxico, Huíla, Namibe and Luanda). A total of 131 districts were mapped. Parasitological examinations, knowledge attitudes and practices questionnaires were implemented in 640 public schools.

School selection procedures

An average of five schools per district were selected but the number of schools selected by district was determined according to population data and the geographical area to be covered. The total number of schools per district ranged from 1 (in unpopulated areas and/or in highly concentrated urban areas) to 13 (in large geographical areas).

School selection was done in two stages: in the first instance, simple random sampling was conducted to select a defined number of schools per district. Then, the list was assessed with direction from local authorities to verify the geographical spread of schools selected across the district. Schools selected close to one another were purposively replaced by schools in locations known to be in areas of increased risk for SCH transmission. The proximity to fresh water sources (river, lakes, lagoons or swamp areas) were considered for this exercise to ensure oversampling in these specific areas, as these provide the ideal ecological conditions for SCH transmission and are recommended as areas where mapping should be conducted30.

Study participants

Fifty children per school, 25 males and 25 females aged between 10–14 years old were invited to participate the day before the survey. School directors were asked to provide a list of all students to ensure systematic random selection.

For inclusion, only school-aged children resident in the study area for at least 2 years were considered to participate. Informed consent was requested of the child’s parents the day before and only those carrying signed informed consent were included in the study.

Children who had taken any antiparasitic drug in the previous 6 months (particularly Albendazole, Mebendazole, Praziquantel, Ivermectin) were not included in the survey.

Parasitological diagnosis

All children were provided with two plastic pots and requested to provide fresh stool and a urine sample. Kato Katz technique was used for analysing stool samples and urine filtration was used for the analysis of urine.

Kato Katz is a WHO reference technique for detecting and determining infection intensity for STH and Schistosoma mansoni allowing identification and quantification of these parasites [31] Microscopy using the Kato Katz technique requires fresh stool specimens, therefore analysis of specimens was conducted on site. The technique consisted of a microscopic examination of a sample of stool to examine the number of eggs in the faeces. All samples were collected, processed, and examined on the same day. All eggs were counted within one hour of preparing the slides. A single slide per student was prepared and reading was done once in the day of the collection as recommended for operational mapping30.

Urine filtration microscopy is the WHO standard technique for evaluating Schistosoma haematobium infection. A microscopic examination of a filter was used to collect the eggs of S. haematobium from 10 ml of urine. Macro-haematuria was visually inspected prior to the microscopic analysis of each sample.

Data collection and management (ESPEN Collect)

Data was collected though standard questionnaires using the ESPEN collect tool. The tool was developed by the Expanded Special Project for the Elimination of Neglected Tropical diseases (ESPEN) to allow collection of survey data and inform school and administrative level prevalence in real time. The tool was shaped to integrate key parameters under assessment and adjusted to Angola’s geographical regions by adding administrative boundaries to the mapping modules. ESPEN collect also allowed the generation of non-identifiable unique identifiers for every single child providing a useful resource to link parasitological data with school conditions and Knowledge, Attitudes and Practices (KAP) data.

The ESPEN Collect had four main questionnaires that were filled by a dedicated data manager in each team who was responsible to input all information of the survey.

Questionnaire 1. School Information sheet–This questionnaire collected information about school population (number of Students/teachers); Water source availability in the school and type of source to have water in the school; existence of freshwater bodies around the school; Presence and type of sanitation structure in the school; Presence and type of handwashing station in the school;

Questionnaire 2: Kato Katz sheet: This form provided collected individual data per student on the number of eggs counted of each species found in the slide (S. mansosi, Ascaris Lumbricoides, Trichuris Thricuria, Hookworm and others)

Questionnaire 3: Urine Filtration sheet: Also provided individual data per student about Macroscopic looking of the sample; Volume of Urine filtered and Number of S. haematobium eggs.

Questionnaire 4: Students’ hygiene and risk behaviours: This questionnaire was used to all enrolled children and collected information about children gender, age, and hygiene behaviours such as usual place of defecation and freshwater bodies regular contact.

School location details were recorded in all questionnaires alongside. A single student identification code was generated for each participant that was used in all forms. This unique identified was used to merge the four datasets generated and analyse data gathered.

Statistical analysis

Data were merged, cleaned, and analysed using Stata version 16 (College Station, TX: StataCorp LLC.). Prevalence (percentage and 95% confidence interval (CI)) and intensity of each infection (based on specified WHO thresholds30), any STH and any SCH infection were calculated based on the presence of eggs present in stool or urine samples, as appropriate, and presented by province and district (S1 and S2 Files).

STH and SCH risk for each district was determined using the calculated prevalence and based on the specified WHO thresholds [31]. The risk was mapped on a geographical map of Angola using ArcGIS version 10.3 (ESRI, Inc., Redlands, USA).

Finally, logistic regression using robust standard errors which accounted for clustering by school was used to explore whether the presence of a latrine or water source in the school was associated with STH or SCH infection, respectively. Models were adjusted for demographic factors including age, sex and province.

Results

Over the survey period, 31,938 children were sampled from 640 schools across 131 districts in Angola and covered 15 of the 18 provinces across the country. Children were aged between 10 and 14 with a median age of 12 (interquartile range: 11–13) (Table 1).

Table 1. Geographical Distribution of sampled schools and children and key characteristics of the sample.

Province Children Schools Male Female
31938 640 15966 15972
Bengo 1549 (4.9%) 31 (4.8%) 780 (50.4%) 769 (49.6%)
Benguela 2150 (6.7%) 43 (6.7%) 1082 (50.3%) 1068 (49.7%)
Bie 2373 (7.4%) 48 (7.5%) 1192 (50.2%) 1181 (49.8%)
Cabinda 1150 (3.6%) 23 (3.6%) 575 (50.0%) 575 (50.0%)
Cuando Cubango 1850 (5.8%) 37 (5.8%) 925 (50.0%) 925 (50.0%)
Cunene 2100 (6.6%) 42 (6.6%) 1050 (50.0%) 1050 (50.0%)
Huila 3650 (11.4%) 73 (11.4%) 1826 (50.0%) 1824 (50.0%)
Kwanza Norte 2372 (7.4%) 48 (7.5%) 1195 (50.4%) 1177 (49.6%)
Kwanza Sul 2750 (8.6%) 55 (8.6%) 1377 (50.1%) 1373 (49.9%)
Luanda 1300 (4.1%) 26 (4.1%) 648 (49.8%) 652 (50.2%)
Lunda Norte 2450 (7.7%) 49 (7.7%) 1226 (50.0%) 1224 (50.0%)
Lunda Sul 1544 (4.8%) 31 (4.8%) 745 (48.3%) 799 (51.7%)
Malanje 2900 (9.1%) 58 (9.1%) 1449 (50.0%) 1451 (50.0%)
Moxico 2800 (8.8%) 56 (8.8%) 1396 (49.9%) 1404 (50.1%)
Namibe 1000 (3.1%) 20 (3.1%) 500 (50.0%) 500 (50.0%)

Prevalence of SCH infection

Overall, the sampled prevalence of any SCH infection amongst SAC children was 13.2% [95% CI: 12.8–13.5] with S. haematobium being the most prevalent species (12.6% [95% CI: 12.2–12.9]) compared to S. mansoni (0.9% [95% CI: 0.8–1.0]). The prevalence of any SCH infection was highest in Huila (32.3%), followed by Benguela (19.3%), Malanje (18.3%), and lowest in Lunda Sul (1.8%). Although S. haematobium was prevalent across all 15 sampled provinces, S. mansoni was only prevalent across 10 provinces. District specific prevalence with respective gender disaggregation can be found in S1 File.

When calculating risk of SCH infection, only two districts had a high risk (>50% prevalence) of SCH infection, 59 with a medium risk of SCH infection (10–50% prevalence) and 57 with a low risk of SCH infection (<10% prevalence). No SCH infections were reported from nine districts (Fig 1).

Fig 1. Schistosomiasis risk (derived from Schistosomiasis prevalence) across 15 provinces of Angola (2018/2019).

Fig 1

(Source: Ministry of Health Angola).

Prevalence of STH infection

The prevalence of any STH infection was 24.1% [95% CI: 23.7–24.6] with A. lumbricoides being the most prevalent species (19.0% [95% CI: 18.6–19.5]) followed by Hookworms (5.8% [85% CI: 5.6–6.1]). T. trichiura (1.6% [95% CI: 1.4–1.7]) was the least prevalent species. The prevalence of any STH infection was highest in Kwanda Norte (69.7%), followed by Malanje (55.9%), Lunda Norte (50.5%), and lowest in Namibe (0.8%). Five provinces (Bengo, Kwanza Norte, Lunda Norte, Lunda Sul and Malanje) had a prevalence of >20% (moderate risk) of A. lumbricoides. Only two provinces (Malanje and Moxico) had a moderate risk of Hookworm infection. All provinces had a low risk (<20% prevalence) of T. trichiura. District specific prevalence with respective gender disaggregation can be found in S2 File.

When calculating risk of STH infection by district, 30 districts had a high risk (>50% prevalence), 24 with a medium risk (20–50% prevalence) and 58 with a low risk (<20% prevalence) of STH infection. No STH infections were reported in 15 districts across the country (Fig 2).

Fig 2. Soil Transmitted Helminthiasis risk (derived from STH prevalence) across 15 provinces of Angola (2018/2019).

Fig 2

(Source: Ministry of Health Angola).

School data

School questionnaires were available for 639 schools (no data was recorded for one school in Namibe province), and therefore included in the following analyses. Only 30% (189/639) of schools reported having a water source in the school. For the majority of these schools, the water source was a protected fountain (26.5%; 50/189) or tap water (25.4%; 48/189) (S3 File).

Approximately 60% (385/639) of schools reported having latrine in the school grounds, with 37.7% (145/385) being a paved latrine, 26.8% (103/385) a non-paved latrine, 21.8% (84/385) a latrine with a flush and 12.7% (49/385) a ventilated improved pit (VIP) latrine. However, the majority (73.0%; 281/385) of schools with an available latrine reported never having water or toilet paper to use after using a latrine.

Student behaviour questionnaire

Analysis showed a large proportion of missing data, discrepancies and conflicting answers. For that reason, these results are presented in S4 File but were not considered robust enough to be included in further analysis.

Infection risk associated with latrine/water source in school

There was no association between the presence of a latrine (odds ratio (OR): 1.21 [95% confidence interval: 0.90, 1.62]) or water source (OR: 0.90 [0.67, 1.19]) in the school and SCH infection. This remained true in a multivariable logistic model (Table 2).

Table 2. Logistic regression assessing the association between presence of latrine or water source in the school and SCH and/or STH infection adjusted for age, sex and province.

Univariable Multivariable
OR (95% CI) p-value OR (95% CI) p-value
SCH infection
Latrine in school No 1 0.21 1 0.72
Yes 1.21 (0.90, 1.62) 1.04 (0.83, 1.31)
Water source in school No 1 0.45 1 0.33
Yes 0.90 (0.67, 1.19) 0.88 (0.68, 1.14)
STH infection
Latrine in school No 1 0.005 1 0.72
Yes 0.69 (0.54, 0.89) 1.04 (0.83, 1.31)
Water source in school No 1 0.05 1 0.33
Yes 0.75 (0.57, 0.99) 0.88 (0.68, 1.14)

Although there seemed to be a reduced risk of STH infection with the presence of a latrine (OR: 0.69 [0.54, 0.89]) and water source (OR: 0.75 [0.57, 0.99]) in the school, these associations did not remain after adjustment for age, sex and province (Table 2).

Discussion

This SCH and STH mapping effort constitutes a landmark for NTD control in Angola. This has been the first country wide mapping exercise that sampled and collected SAC children data across several provinces to estimate the prevalence of these diseases. Despite the mapping exercises conducted in 2005 [26] and later in 2014 [29] and 2021 [9], this is the first mapping at country level that consistently follows WHO guidance for SCH and STH mapping in Africa [30].

Geographical distribution of SCH is consistent with historical data identifying high prevalence of this disease across Bié, Huila, Benguela, Bengo and Luanda provinces [9,10,1318]. This is also in line with the 2005 mapping data that identified a higher prevalence of SCH across the central plateau [26]. S. haematobium prevalence is consistently higher than S. mansoni across these areas which is a consequence of the focal nature of SCH transmission, its association with human contact with infested water and the existence of a specific intermediate snail host [32].

Higher prevalence of STH was found in the northern provinces of Kwanza Norte, Malanje, Lunda Norte and Lunda Sul, with some schools mapped noting 100% of SAC infected with at least one STH. Ascaris has been the main infection found across these provinces, but Hookworm was frequently identified across Lunda Sul, Moxico and in Malanje, where there is a historical record of the disease [11,14]. These findings highlight the need to tailor communication interventions in these areas, particularly in impoverished rural areas where children tend to walk barefoot, a known risk factor for hookworm infection [33,34].

Less than a third of schools reported to have a water source in the school perimeter. Of these, only half had safe water source (protected fountain or tap water). Such results are in line with existing data about access to basic service water in Angola [3537]. Similarly, sanitation information from schools mapped is aligned with existing information about sanitation access in schools in Angola [37]. These findings raise the need to improve water and sanitation conditions for SAC across the country. The low proportion of schools with sanitation equipment that had water or toilet paper to use after using a latrine suggests the need to invest in better sanitation equipment to ensure handwashing post defecation. Since poor WASH conditions are associated with increased risk of both SCH and STH transmission [38,39], it is essential to look at NTD control as an integrated approach that includes improvements of water and sanitation access and conditions in schools.

4041–44When controlling for age, sex and province, the presence of water and latrine in school was not associated with STH nor with SCH infections. This may be related to the absence of water and sanitation conditions in communities where children live. Children may have access to these conditions in schools but have limited or no access to adequate water and sanitation at home, a problem that has been previously identified [40]. Another major contributor may be the limited use of existing sanitation structures in schools [37]. Unfortunately, due to the high proportion of missing behavioural data, it was not possible to accurately assess these. But, when looking at the proportion of children reporting to urinate or defecate in school latrines, approximately only a fifth of children report to do so. WASH in school is essential to provide essential infrastructure, to foster its use and the adoption of healthy sanitation behaviours. This is not new as the requirement for investments in WASH in schools in Angola have been raised historically by UNICEF [37].

Results obtained by this mapping are essential to adequately plan MDA campaigns and ensure geographical areas are targeted based on the need. The Angola NTD Masterplan 2021–2025 [41] (final version awaiting ministerial approval) integrates this mapping data and projects its long-term results in line with WHO roadmap [1]. However, the main identified risk to attain those results is linked to the chronical lack of support to NTD activities in Angola. So far, financial support to conduct MDA has been provided by WHO and The MENTOR Initiative (through an End Fund Grant). MDA activities have been implemented across seven provinces with gradual appropriation of activities from several district and provincial health and education authorities over time. Nevertheless, mapping results “demand” the rapid scale up of MDA to several districts. For STH, 30 districts should be targeted bi-annually and 24 targeted annually corresponding to an estimated total of 2.650.000 SAC treated annually. For SCH, 2 districts should be targeted annually and 65 targeted at least once in 5 years, in an estimated total of 2.950.000 SAC children to be treated (Table 3). These treatment efforts need to be integrated with community level MDA, particularly where overlap of treatment with Albendazole is foreseen. However, as lymphatic filariasis mapping data is outdated, it is hard to accurately integrated these strategies.

Table 3. Number of districts in each province to be targeted for MDA according to mapped risk.

Província N SCH STH
Low Medium High Low Medium High
Bengo 6 2 (33.3%) 4 (66.7%) - 2 (33.3%) 1 (16.7%) 3 (50.0%)
Benguela 10 3 (30.0%) 6 (60.0%) - 7 (70.0%) - -
Bie 9 6 (66.7%) 3 (33.3%) - 9 (100.0%) - -
Cabinda 4 2 (50.0%) 1 (25.0%) - 2 (50.0%) 2 (50.0%) -
Cuando Cubango 9 6 (66.7%) 2 (22.2%) - 5 (55.6%) - -
Cunene 6 3 (50.0%) 3 (50.0%) - 6 (100.0%) - -
Huila 14 2 (14.3%) 10 (71.4%) 2 (14.3%) 8 (57.1%) - -
Kwanza Norte 10 4 (40.0%) 5 (50.0%) - - 1 (10.0%) 9 (90.0%)
Kwanza Sul 12 5 (41.7%) 7 (58.3%) - 8 (66.7%) 4 (33.3%) -
Luanda 9 5 (55.6%) 3 (33.3%) - 4 (44.4%) 1 (11.1%) -
Lunda Norte 10 5 (50.0%) 1 (10.0%) - - 4 (40.0%) 6 (60.0%)
Lunda Sul 4 2 (50.0%) - - - 3 (75.0%) 1 (25.0%)
Malanje 14 3 (21.4%) 11 (78.6%) - - 3 (21.4%) 11 (78.6%)
Moxico 9 6 (66.7%) 1 (11.1%) - 4 (44.4%) 5 (55.6%) -
Namibe 5 3 (60.0%) 2 (40.0%) - 3 (60.0%) - -

One of the major limitations of this study is related to the sampling procedures and its impact on calculating SCH prevalence at sub district level. Sampling procedures were used to estimate prevalence at district level. Due to the focal nature of SCH, WHO recommends sub district estimates for SCH prevalence [42] and produced a tool to extrapolate prevalence at the sub-district level out of district level results. Such tool has also been adopted in Angola to refine mapping results. Another operational limitation of this was the non-inclusion of three provinces: Huambo, Uige and Zaire. These provinces have been mapped in 2014 and MDA have been implemented since. Considering that mapping should occur after 5 years of MDA, it was agreed that an impact assessment would take place in 2020 (delayed to 2021 due to the COVID-19 pandemic).

The use of single stool and urine samples for estimating the prevalence is also a major limitation to interpret the findings. The Kato Katz technique has recognized accuracy limitations particularly for low intensity infections. Therefore, it would have been preferable to collect several samples over time to improve accuracy [43]. However, considering the scope and size of the mapping needed to characterize STH and SCH prevalence in Angola and the available resources, such methods would have been unfeasible to implement across the country.

The inability to explore individual hygiene behaviours constitute a major challenge in order to fully understand STH and SCH risk behaviours of SAC in Angola. Nevertheless, this descriptive analysis, exploring the presence of a latrine or water source in the school provides important insights about key regions that have the highest risk of contracting SCH and STH. These should be targeted through information campaigns aiming to reduce well identified risk behaviours such as poor handwashing practices, open defecation, walking barefoot and bathing in rivers, dams, or lakes.

Since egg counting procedures and recording were not consistently done across all provinces, it was not possible to compute infection intensities. This poses a limitation to follow up the impact of NTD control interventions on infection intensity over time. In addition, it was not possible to map pre-SAC or other risk groups which constitutes a limitation to understand better transmission patterns across the whole Angolan population, including the role of adults in transmission of STH and ACH. Previous studies identified pregnant women to be at risk of infection in Angola [9]. Future research in Angola should consider the inclusion of adults that are not generally targeted in SCH and STH control interventions.

Conclusions

This first ever STH and SCH mapping in Angola achieved it main objective of quantifying the prevalence and distribution of these infections across the country. Results are of vital importance to map the prevalence and geographical distribution of these diseases and plan adequate interventions that support NTD control in Angola and contribute to WHO 2030 defined NTD control targets. Water and sanitation conditions in schools across Angola are still scarce and may be a significant factor contributing for the high endemicity of some NTD in Angola.

Supporting information

S1 File. Schistosomiasis haematobium, Schistosomiasis mansoni and Any Schistosomiasis prevalence (and 95% CI) by province and district with gender disaggregation.

(XLSX)

S2 File. Ascaris Lumbricoides, Trichuris, Hookworm and any Soil Transmitted Helminth prevalence (and 95% CI) by province and district with gender disaggregation.

(XLSX)

S3 File. WASH conditions in schools sampled.

(XLSX)

S4 File. Individual students practices related to WASH.

(XLSX)

Acknowledgments

The authors would like to thank all lab workers and data managers who significantly contributed to ensure the implementation of field work. Likewise, to all logistic staff involved (drivers, mobilizers) who supported daily field activities. The authors also acknowledge all the Provincial and Municipal authorities support to the implementation of this mapping and, to Education and Health departments at provincial and district level who facilitated all contacts and, in the vast majority of the cases provided housing for field teams in remote settings. A major appreciation should also be given to all School Directors and teachers that contributed in a very positive way to make this mapping happen as they played a major role in mobilizing parents and children to enrol in the mapping. Finally, the authors would like to thank all parents and children engaged in the mapping for their vital contribution to better understand neglected tropical diseases in Angola.

Data Availability

Data cannot be shared publicly as it is MoH Angola data. Data are available from the MoH Institutional Data Access via geral@inis.ao or visit https://www.inis.ao/index.php/contactos.

Funding Statement

This mapping was funded by ESPEN/WHO (https://espen.afro.who.int/). The study was also partly funded by The END Fund under the current NTD country support program under implementation by The MENTOR Initiative. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0010458.r001

Decision Letter 0

Christine M Budke

9 Aug 2021

Dear Mr Lopes,

Thank you very much for submitting your manuscript "Mapping of Schistosomiasis and Soil-Transmitted Helminths across 15 provinces of Angola" for consideration at PLOS Neglected Tropical Diseases.

When conducting the initial review of your submission, I noticed that there were a number of indications that the submitted version of the document was not the final version. For example, the submitted version has at least one reference place holder (i.e., [ref]), questions from co-authors left in the text associated with Table 1, supplementary materials referenced in the text as Appendix x, inconsistent use of abbreviations, etc. I would ask that you please address these issues and submit a revised version of your paper. Once an updated version has been submitted, the paper will be considered for review. Please note that this is not a guarantee that your manuscript will be accepted for publication.

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.

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Sincerely,

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PLOS Neglected Tropical Diseases

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

When conducting the initial review of your submission, I noticed that there were a number of indications that the submitted version of the document was not the final version. For example, the submitted version has at least one reference place holder (i.e., [ref]), questions from co-authors left in the text associated with Table 1, supplementary materials referenced in the text as Appendix x, inconsistent use of abbreviations, etc. I would ask that you please address these issues and submit a revised version of your paper. Once an updated version has been submitted, the paper will be considered for review. Please note that this is not a guarantee that your manuscript will be accepted for publication.

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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.

PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0010458.r003

Decision Letter 1

Christine M Budke

25 Nov 2021

Dear Mr Lopes,

Thank you very much for submitting your manuscript "Mapping of Schistosomiasis and Soil-Transmitted Helminths across 15 provinces of Angola" 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.

We cannot make any decision about publication until we have seen the revised manuscript and your response to the reviewers' comments. Your revised manuscript is also likely to be sent to reviewers for further evaluation.

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

[1] A letter containing a detailed list of your responses to the 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.

Please prepare and submit your revised manuscript within 60 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email. Please note that revised manuscripts received after the 60-day due date may require evaluation and peer review similar to newly submitted manuscripts.

Thank you again for your submission. 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,

Christine M. Budke

Deputy 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: Yes

Reviewer #2:

The data availability statement is incorrect because when it says where can the data be found, the authors have put these data cannot be shared.

Line 11 of the abstract says 31,938 children in the study but in line 10 of the author summary says 13.000 which I presume is supposed to be 13,000 but is also inconsistent with the abstract or unclear if the correct number – what is the almost 32,000 if not the number of children included? In future do not restart page numbers for each section of the document. It makes referencing the correct part difficult, especially seeing as you have no page numbers.

Introduction Line 7 – it is also to do with water contact patterns, sociodemographic factors etc, these all contribute to the force of infection.

Line 13 – you have referred to these as abbreviations above so SCH and STH should be abbreviations consistently. Also, schistosomiasis is the disease so does not need to be capitalised, but Schistosoma haematobium on line 19 has not been taxonomically declared before and should in this instance be spelt out with a capitalised S.

Lines 24-25 – What do you mean by this sentence? All prevalence/ burden measures in any location are estimates as nowhere is the whole community sampled.

Line 7 page 2 of your introduction – is MENTOR an acronym?

The introduction would benefit from reference to the maps. It is quite listy in terms of locations and previous mapping efforts. Perhaps in the introduction, some guidance from the authors for the readers as to whether the overall prevalence and intensities of infections for schistosomiasis or STH are going up or down? Why is this mapping effort so important? As it stands, it seems like there have been regular and ongoing efforts to map these diseases.

Line 20 School selection criteria – close not closed?

Line 24 School selection criteria – some clarification for why you wanted to oversample in these locations would be beneficial.

Line 10 Parasitological diagnosis – mansoni should not be capitalised. It has also not been taxonomically described yet in the text and should be fully spelt out in this instance.

Line 15 Parasitological diagnosis – this is not true. The Kato-Katz method lacks sensitivity, egg excretion from the human host is highly over dispersed and does not necessarily reflect the density of female worms – there are a few hypotheses for this including density dependent reproduction, host acquired immunity and worm senescence. As it is essentially incorrect, please remove this sentence. Further to this, you do not explain at all how many stool samples you use, or over how many days (Lamberton, 2014). The methods generally lack any useful detail and give too much opinion.

Lines 24-33 are superfluous. If you really want to include them put them in an appendix but for the purpose of the main text I would remove them.

Lines 1-9 ESPEN data collection – Rather than describing what the ESPEN tool is, I would like to understand clearly and concisely what it was used to collect. This is not clear from the text. This can be significantly streamlined.

Line 21 Statistical Analysis – you have a (ref) that I presume should be a reference.

Line 30 Statistical Analysis – when you say clustering here, do you mean that the school was considered as a random effect in the model? Does this mean you did no analysis on infection intensity despite having all of these egg counts? I think this is a really important point. You could have high prevalence of low intensity infections. Furthermore, we know that the KK method performs poorly in low prevalence and low infection intensity settings – without an analysis on the intensities how can we really tell if this mapping is reflective of true infection distribution? I’d be likely to think there are more infections than this has detected if the intensities are low and maybe more likely to think it has done a good job at characterising infections if the counts are very high. With such huge sample sizes I am also unsure why you needed to do a univariate analysis first. This method notoriously produces spurious results. Did you not include any interactions or random effects either? I feel the statistical analysis here is either lacking effort and rigour or maybe lacking a more substantial technical description? I think I will not understand which it is until at least a more detailed technical description of the analysis is provided. Indeed, if this is such an important mapping effort, then peoples quality of life can depend on these results meaning statistical rigour is essential. Also, I wonder what the malaria treatment situation is given the prevalence of malaria in Angola and that malaria treatment has anti-schistosomal effects. “Data” is a plural word so reporting should be “no data were” or “not data are” rather than “no data was” and “no data is”.

Discussion line 21 – do you think communication is needed for impoverished children to wear shoes or do you think this is a funding issue where funds should be diverted to enable shoe wearing? I think you really need to discuss the fact that egg-based diagnostics, particularly for SCH, is simply not an adequate tool for capturing true prevalence and intensity measures. This is not mentioned at all in your discussion and is a major problem. Given that there is no description for how many counts per stool over how many days, I am presuming also that just one count was done. This is also inadequate and grossly underestimates prevalence and infection intensity. These are major limiting factors to the credibility of the estimates provided. Also, in the context of the new WHO roadmap, what is the part played by animals in the maintenance of S. haem? Given recent work that has been published (Borlase, 2021 Leger, 2020) this deserves a comment in the discussion. You also have no comment of the fact that you only sampled children. Adults can harbour incredible infections and manifest chronic morbidity more often. In such instances then, who is really suffering the most from infection, children with high egg shedding rates, or adults with low egg shedding rates but high levels of morbidity (caused by the eggs not shed). you say that the WHO give guidance for taking district level estimates and turning them into subdistrict estimates. What is this method?

Reviewer #3: Authors made a good attempt in investigating a very important issue on evidence guided decision making. however, further clarity on the how the results reflect on the objective is required. In terms of the results, authors needs to bring out variate analysis output gender and age variations especially at province levels.

The sample size is sufficient enough for this types of surveys an perceived adequate to prove useful information.

No ethical issues of significance were noted, the authors however needs to demonstrate coherently how consent have been given, written, or signed, could the parents read, or who was available to explain to parents to seek consent, does consent seeking involve translations. was there any participants excluded for reasons of non consent.

The objective of this survey, which is stated as "mapping the epidemiology of SCH and STH" should be defined, to give give a grasp of what the authors meant by mapping the epidemiology of SCH and STH.

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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: Yes

Reviewer #2: (No Response)

Reviewer #3: Table 1, 2 and 3, need improvement on the appropriate titles, and content. Table 1 could incorporate more information on demographics of the study participants at province or municipal levels.

The presentation of the results and the discussion should relate to the objective including how it will guide treatment arrangements.

How does the integrated treatment relate to or affect the wider community based MDA is not very clear.

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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: Yes

Reviewer #2: (No Response)

Reviewer #3: Authors should be concise but conclusive on the final take on the extent in which the objectives of the study had been achieved and how it will be used to guide strategic prevention and control strategies.

The public health relevance of the study had been achieved in practice. Although the information presented should be more coherent in both writeup style, arrangement and flow of the information being presented and expressions.

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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: • Page 9, line 3 – “individuals’” should be “individual’s”

• Throughout: “S. Haematobium” should be “S. haematobium”. Same with S. Mansoni.

• Throughout: “Schistosomiasis” should be “schistosomiasis” unless at the start of a sentence.

• Page 9, line 35, recommend changing “global” to “nationwide”.

• Page 10, line 4: “remainder” should probably be “remaining”

• Page 10, line 7: is “municipalities” here the same as “districts”?

• Page 14, lines 5-6: “Informed Consent forms were sought near participants parents” should probably be “Informed Consent forms were sought from participants’ parents”.

• Page 14, line 6: “Team elements” might be better as “Team members” or “Team leaders”.

• Page 16, lines 21 and 22: “pavement” might be better as “paved”.

• Page 20, line 34: “age’ could be removed.

• Page 21, line 3: “prevalence sub-district level” should probably be “prevalence at the sub-district level”

Reviewer #2: (No Response)

Reviewer #3: Line numbering was set by the authors to be repetitive per page and made review especially making reference to specific lines very cumbersome. Authors should set line numbers to be continuous instead.

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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: This is a well written and very interesting paper looking at the distribution of SCH and STH in Angola. The sample size is extensive – stretching to 640 schools, 32,000 children across 131 districts. These data will clearly be of use in planning SCH and STH interventions in the country and as a staging post to 2030 targets.

A few questions outlined below, most are minor.

Comments

• Abstract – results. When saying infection was related to age and sex, I’d recommend making clear in what direction. E.g. older people more likely to be infected. Males more likely to be infected. This is included in the results section, add to abstract.

• Abstract – mention whether you are referring to S.mansoni or S.haematobium.

• Author summary – this mentioned a sample size of 13,000 children, but 32,000 are referenced in the abstract. Which is accurate?

• Methods: For children indicating that they had taken parasitic drugs in the last six months, how many were there?

• Methods: “Schools selected that were closed to each other were purposively replaced by schools in locations known to be in areas of increased risk for Schistosomiasis transmission.” I think that’s a fine way to proceed, but we should be aware that it doesn’t give rise to unbiased estimates of prevalence.

• Methods: Student behavior questionnaire: agree that if data are not robust enough, they should not be used for analysis. What is the reason for that – due to students not understanding the questions? Methodological flaws?

• Methods: For age, how is the odds ratio calculated. For each additional year of age? Or comparing age categories?

• Page 16, lines 29-31. Interesting that children were less likely to have SCH infection if they had STH infection (but not in the multivariate analysis). Why do the authors think that is?

• Page 20, lines 17-19: “Overall, data indicate that WASH in school investments are essential to provide essential infrastructure and to foster its use and the adoption of healthy sanitation behaviours”. I agree that there are so many reasons why school WASH infrastructure should be improved. But this paper does not show SCH / STH infection to be one of them.

• Could consider bringing Additional File 5 (number of districts in each province to be targeted for MDA) into main body. But not compulsory.

Reviewer #2: (No Response)

Reviewer #3: This survey is an important activity as part of the NTD elimination roadmap, and information generated will be very useful in guiding efforts in intervention. What the authors need is review the writing style, grammar, expression, flow and other typographical errors. Analysis and results should be more extensive in portraying province and municipality variance for ages and sexes and the strategy for treatment and other intervention like WASH, on the basis of evidence of level of prevalence high, medium and low.

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Reviewer #1: Yes: Michael French

Reviewer #2: No

Reviewer #3: Yes: Yaya Camara

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

Attachment

Submitted filename: pntd-d-21-01157-r1-reviewer.docx

PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0010458.r005

Decision Letter 2

Christine M Budke

10 Apr 2022

Dear Mr Lopes,

Thank you very much for submitting your manuscript "Mapping of Schistosomiasis and Soil-Transmitted Helminths across 15 provinces of Angola" 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,

Christine M. Budke

Deputy 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: I am of the opinion the the authors should limit the objective to the distribution of the said diseases, something like the prevalence and distribution. The term burden seem more complex to be established and seems inadequately addressed by the data presented.

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

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: (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 #2: (No Response)

Reviewer #3: (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 #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: This is the second time I have handled this manuscript. Given the satisfactory response to the original review I just have a few additional minor things:

First, I totally appreciate the amount of effort that has gone into this mapping. My commentary on the lack of sensitivity with a single Kato-Katz was not a slight on your effort but on the continued recommendation from large bodies such as WHO, for its use, and thus a continued lack of financial support provisioned for improved diagnostics and labour. The 2030 goal is ambitious and if we cannot truly understand the dynamics how will it be possible to reach. As such, I hoped to see in the original version, a more thorough discussion of this as this is where experts such as yourselves can have your say and highlight this dire need. Indeed you have responded to my request for more of this in the discussion with a small section but I stand by my original review comment - that there are additional complexities to control that the WHO mapping protocol just does not capture. I do not expect you to add more to the discussion at this point, the manuscript is fine as it is, but just food for thought.

Line 17 Parasitological diagnosis - remove the fullstop after Schistosoma

Line 23 ESPEN collect section - Expanded not Espanded

Reviewer #3: (No Response)

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

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 #2: No

Reviewer #3: Yes: Yaya Camara

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.

Attachment

Submitted filename: ReviewerComments-PNTD-D-21-01157-R2.docx

PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0010458.r007

Decision Letter 3

Christine M Budke

1 May 2022

Dear Mr Lopes,

We are pleased to inform you that your manuscript 'Mapping of schistosomiasis and soil-transmitted helminthiases across 15 provinces of Angola' 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,

Christine M. Budke

Deputy Editor

PLOS Neglected Tropical Diseases

Christine Budke

Deputy Editor

PLOS Neglected Tropical Diseases

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

PLoS Negl Trop Dis. doi: 10.1371/journal.pntd.0010458.r008

Acceptance letter

Christine M Budke

20 Jun 2022

Dear Mr Lopes,

We are delighted to inform you that your manuscript, "Mapping of schistosomiasis and soil-transmitted helminthiases across 15 provinces of Angola," 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

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 File. Schistosomiasis haematobium, Schistosomiasis mansoni and Any Schistosomiasis prevalence (and 95% CI) by province and district with gender disaggregation.

    (XLSX)

    S2 File. Ascaris Lumbricoides, Trichuris, Hookworm and any Soil Transmitted Helminth prevalence (and 95% CI) by province and district with gender disaggregation.

    (XLSX)

    S3 File. WASH conditions in schools sampled.

    (XLSX)

    S4 File. Individual students practices related to WASH.

    (XLSX)

    Attachment

    Submitted filename: Response letter.docx

    Attachment

    Submitted filename: pntd-d-21-01157-r1-reviewer.docx

    Attachment

    Submitted filename: 20220214_Response to reviewers.docx

    Attachment

    Submitted filename: ReviewerComments-PNTD-D-21-01157-R2.docx

    Attachment

    Submitted filename: 20220424_Response to reviewers.docx

    Data Availability Statement

    Data cannot be shared publicly as it is MoH Angola data. Data are available from the MoH Institutional Data Access via geral@inis.ao or visit https://www.inis.ao/index.php/contactos.


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