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A holistic approach to address
female genital schistosomiasis in
Ghana and Madagascar: the FGS
Accelerated Scale
Together Package
Alison Krentel
1,2
*, Kazeem Arogundade
2
,
Mbolatiana Raharinivo
3,4
, Joseph Opare
5
,
Clara Fabienne Rasoamanamihaja
6
,
Faly Hariniaina Randrianasolo
3,4
, Maxwell Ayindenaba Dalaba
7
,
Mustapha Immurana
7
, Isis Umbelino-Walker
8,9
,
Caroline Pensotti
8,9,10
, Moussa Sangare
1,2
, Kruti Patel
1
,
Julie Jacobson
8,9
and Margaret Gyapong
7
1
School of Epidemiology and Public Health, Faculty of Medicine, University of Ottawa, Ottawa,
ON, Canada,
2
Bruyere Research Institute, Ottawa, ON, Canada,
3
K’Olo Vanona Association,
Antananarivo, Madagascar,
4
National Institute of Public and Community Health, Ministry of Public
Health, Antananarivo, Madagascar,
5
NTD Programme, Disease Control Unit, Public Health Division,
Ghana Health Service, Accra, Ghana,
6
NTD Programme, Ministry of Public Health,
Antananarivo, Madagascar,
7
Institute of Health Research, University of Health and Allied Sciences, Ho,
Volta Region, Ghana,
8
Bridges to Development, Vashon, WA, United States,
9
Bridges to Development,
Geneva, Switzerland,
10
Unlimit Health, London, United Kingdom
Women and girls who have been infected with the blood fluke Schistosoma
haematobium can experience the chronic form of urogenital schistosomiasis,
called female genital schistosomiasis (FGS). Some FGS symptoms resemble
sexually transmitted infections. As a result, women and girls seeking treatment
are often misdiagnosed and stigmatized. The FGS Accelerated Scale Together
(FAST) Package project implemented a holistic approach to address FGS
combining proven interventions in training, mass drug administration,
diagnosis, and treatment as well as community awareness to address FGS in
four selected districts in Ghana and Madagascar. The FAST Package was
supported by an FGS National Committee who provided guidance on
integration at the national level. Using an implementation research design,
researchers worked closely with government counterparts in the programs for
neglected tropical diseases in both countries. Baseline cross-sectional surveys
and qualitative methodologies collected information on schistosomiasis and FGS
awareness, experience with health seeking behaviors and knowledge of
schistosomiasis prevention amongst community members and teachers. FAST
Package interventions included healthcare provider training delivered in online
and in person formats; development of an Educators’booklet to support
schistosomiasis/FGS awareness creation among teachers, healthcare providers
and community members; suspected FGS case detection; and advocacy for the
provision of praziquantel in the primary health care system. Endline results
included a cross-sectional survey and qualitative methodologies amongst
community members and teachers, including Photovoice for women of
Frontiers in Tropical Diseases frontiersin.org01
OPEN ACCESS
EDITED BY
Roch Christian Johnson,
CIFRED UAC, Benin
REVIEWED BY
Humphrey Deogratias Mazigo,
Catholic University of Health and Allied
Sciences (CUHAS), Tanzania
Vanessa Christinet,
Centre Hospitalier Universitaire Vaudois
(CHUV), Switzerland
*CORRESPONDENCE
Alison Krentel
akrentel@bruyere.org
RECEIVED 04 March 2024
ACCEPTED 02 August 2024
PUBLISHED 09 October 2024
CITATION
Krentel A, Arogundade K, Raharinivo M,
Opare J, Rasoamanamihaja CF,
Randrianasolo FH, Dalaba MA, Immurana M,
Umbelino-Walker I, Pensotti C, Sangare M,
Patel K, Jacobson J and Gyapong M (2024)
A holistic approach to address female genital
schistosomiasis in Ghana and Madagascar:
the FGS Accelerated Scale Together Package.
Front. Trop. Dis 5:1395467.
doi: 10.3389/fitd.2024.1395467
COPYRIGHT
© 2024 Krentel, Arogundade, Raharinivo,
Opare, Rasoamanamihaja, Randrianasolo,
Dalaba,Immurana,Umbelino-Walker,Pensotti,
Sangare, Patel, Jacobson and Gyapong. This is
an open-access article distributed under the
terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
reproduction in other forums is permitted,
provided the original author(s) and the
copyright owner(s) are credited and that the
original publication in this journal is cited, in
accordance with accepted academic
practice. No use, distribution or reproduction
is permitted which does not comply with
these terms.
TYPE Original Research
PUBLISHED 09 October 2024
DOI 10.3389/fitd.2024.1395467
reproductive health age exposed to FGS. This paper presents a description of the
FAST Package project, the value of its holistic approach, and selected results from
both countries. It discusses the lessons learnt highlighting some of the challenges
and opportunities for integration within the health system.
KEYWORDS
female genital schistosomiasis (FGS), Schistosoma haematobium, community
awareness, healthcare training, Subsaharan Africa, Ghana, Madagasacar, online training
Introduction
Schistosomiasis is a parasitic disease caused by blood flukes that
is prevalent in tropical and sub-tropical countries, particularly in
areas with inadequate sanitation and poor access to safe drinking
water. It has been reported in 78 countries worldwide, with the
urogenital form of the disease found in Africa, the Middle East, and
Corsica (1). The urogenital form is caused by infection with
Schistosoma haematobium (1). Infection occurs when the larval
forms of the parasite, released by freshwater snails, penetrate the
skin of an individual who has contact with the snail-infested water.
The larvae eventually mature into adult worms, which live in blood
vessels where after mating, the female worm releases its eggs. Some
eggs are released in urine or feces to continue the life cycle, while
others get trapped in body tissues, causing immune reactions and
progressive organ damage (1). Transmission continues when an
infected person passes excreta containing parasite eggs into the
freshwater sources, which later hatch in water and are taken up by
the freshwater snails.
Evidence has shown that differences between males and females
exist for schistosomiasis in terms of vulnerability, exposure, and access
to treatment (2). The gender role of females as it relates to performing
household chores such as fetching water for the family, washing
clothes and dishes, and bathing children puts them at risk of infection
with Schistosoma haematobium (1,3) while for boys, activities like
swimming, fishing and washing vehicles will influence their risk.
In many countries, urogenital schistosomiasis is widely regarded as
a boy’sdisease(4) due to the visible sign of hematuria which boys
detect more easily than girls. This misconception prevents awareness
about the chronic manifestations of untreated Schistosoma
haematobium infection in women and girls (4,5). In females,
Schistosoma haematobium infection can cause a gynecological disease
called Female Genital Schistosomiasis (FGS). FGS presents with vaginal
bleeding, nodules in the vagina, genital lesions, vaginal discharge, and
pain during sexual intercourse, and could result in ectopic pregnancy,
miscarriage, sub-fertility, infertility, spontaneous abortion, and
premature delivery (1,6,7).Anestimatedupto56millionwomen
and girls are affected by FGS (7) and it has been called the “sexual and
reproductive health issue you’ve probably never heard of”(8). Despite
its likely prevalence across Sub-Saharan Africa, awareness of FGS and
its associated sequelae at the community level and health system is
lacking; most medical textbooks do not mention FGS and global and
national policymakers have largely overlooked the disease. Hence
women and girls with FGS are often poorly diagnosed and
misdiagnosed as having sexually transmitted infections by frontline
healthcare providers, leading to stigma, discrimination, unnecessary
investigations, and multiple health care visits (4,6,7,9).
FGS is considered as a risk factor for HPV and HIV due to the
immunological and pathological changes associated with the disease
(6). Studies in sub-Saharan Africa have shown that women suffering
from FGS are at a three-fold increased risk of HIV infection (7,10,
11). African women carry a disproportionate global burden of
cervical cancer and HIV infection (12,13). There is increasing
evidence that controlling one of these three infections (FGS, HIV,
HPV) may decrease the risk of vulnerability and unwanted
outcomes for the two others and improve women’soverall
reproductive health (6,7,9). Each disease has a proven preventive
intervention, from praziquantel treatment for FGS, pre-exposure
prophylaxis, and anti-retroviral therapy for HIV and HPV vaccines
for cervical cancer (9,14).
As recommended by UNAIDS, national programs should
address the gender inequalities that increase the vulnerability of
women and girls in Sub-Saharan Africa to FGS, HIV, and cervical
cancer, through a holistic, integrated, and multisectoral
programming (7). For example, the health care providers
responsible for prevention and screening programs should
consider the higher rates of cervical cancer amongst people living
with HIV and the risks of acquiring HIV associated with FGS (2,6,
7). Age-appropriate management of schistosomiasis, cervical cancer
screening programs, family planning, and other sexual and
reproductive programs are not currently linked. Without breaking
down the siloed approaches of sexual and reproductive health
(SRH) programming, adapting and integrating diagnostic and
treatment protocols for HIV, HPV, and STIs to include FGS and
multifaceted approach at all levels, FGS cannot be effectively
addressed (7,15). Integrating FGS, HIV, and cervical cancer with
existing sexual and reproductive health programs can improve the
health outcomes of girls and women in Africa (14). The policy
framework is already in place to integrate FGS into the primary
health care system and sexual and reproductive health services.
Krentel et al. 10.3389/fitd.2024.1395467
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Sustainable Development Goal 3 seeks to ensure universal access to
sexual and reproductive health, including “information and
education, and integration of reproductive health into national
strategies and programs by 2030”(7). The WHO 2030 NTD
roadmap calls for mainstreaming and greater integration of NTD
approaches into the national health system (1). FGS represents a
unique global health challenge in terms of its scale, neglect, and
positive impact if addressed. Global policymakers have increasingly
advocated for FGS action as a gender, human rights, development,
and reproductive health issue requiring urgent attention (2,16,17).
To address the burden of FGS in girls and women in Ghana and
Madagascar, the FGS Accelerated Scale Together (FAST) Package
or the FAST Package was launched in July 2020 to combine proven
interventions that have been shown independently to improve
detection and clinical outcomes while supporting the uptake and
demand for preventive chemotherapy through mass drug
administration (MDA) to prevent infection. These activities were
supported by the establishment of a FGS National Advisory
Committee to increase communication and collaboration about
FGS with the longer-term goal of integrating FGS management into
existing sexual and reproductive health, clinical training, and care.
The FAST Package covers the life course of a woman, from
prevention of new infections with schistosomiasis and new cases
of FGS to the diagnosis and treatment for existing FGS cases and,
finally, treatment for symptoms of complications due to FGS as a
woman ages. The FAST Package addresses the issue of FGS at the
individual, community, and health system levels (See https://
fastpackage.org/). Each component of the FAST Package works
together to provide a holistic response (See Figure 1).
The FAST Package project aimed to:
1. Increase community members’knowledge about FGS and
its impact on women and girls.
2. Prevent new infections in children and young girls with
schistosomiasis by promoting annual mass drug administration.
3. Increase the capacity of medical personnel to diagnose and
treat FGS.
4. Improve diagnosis and treatment of FGS.
5. Support the National NTD program to integrate FGS into
existing health programming at the Ministry of Health
and partners.
The FAST Package combines a diverse partnership of global
and national partners. The project was supported by Grand
Challenges Canada from June 2020 to September 2022. Grand
Challenges Canada is funded by the Government of Canada and
is dedicated to supporting Bold Ideas with Big Impact®. Match
funding for the FAST package was supported by the Coalition for
Operational Research on NTDs, Merck Global Health Institute,
WHO Expanded Special Project for the Elimination of Neglected
Tropical Diseases, and Unlimit health (formerly the Schistosomiasis
Control Initiative Foundation). This unique partnership allowed
greater visibility for the FAST Package and allowed the learnings
from the project to be transferred to a global level.
The paper describes some of the results and key learnings
related to the project objectives, including a discussion of the
challenges associated with implementation and lessons learned.
Materials and methods
Study design
The FAST Package is an implementation research study using
mixed methods to improve the implementation and delivery of FGS
interventions in selected sites. One of the foundational aspects of
implementation research is to link research and practice through a
close collaboration between researchers and program personnel.
Through continuous feedback loops, data from the research is
presented to the government program for input and adaptation
FIGURE 1
Representation of the FAST Package components.
Krentel et al. 10.3389/fitd.2024.1395467
Frontiers in Tropical Diseases frontiersin.org03
(18). The FAST Package had three distinct phases: a baseline
assessment, an interventional phase, and an endline assessment.
At the baseline and endline phases, cross-sectional surveys were
employed with community members and teachers. Using a
concurrent mixed methods study design (19), in-depth interviews
and focus group discussions were carried out at the same time as the
cross sectional surveys. In the endline phase, photovoice was added
to selected focus group discussions with women of reproductive
health age.
Study setting
The FAST Package was carried out in Ghana and Madagascar.
These two countries were selected based on schistosomiasis
endemicity and on the willingness of the Neglected Tropical
Diseases program managers to see FGS addressed in an integrated
and sustained manner. Study sites included the Weija and North
Tongu Districts in Ghana and the Morondava and Sakaraha
Districts in Madagascar. All selected districts had a reported
schistosomiasis prevalence rate of >50%.
In Ghana, more than 50% of the population is under 25 years,
and about 24% are 25-54 years. Over 95% of Ghanaian children are
enrolled in school. All regions in Ghana are endemic to
schistosomiasis. However, there are specific regions that have a
prevalence rate of over 50% (high-risk regions), and these include
the Volta, Greater Accra, Eastern, and parts of the northern part of
the country.
Weija district is one of the FAST Package districts in the Greater
Accra Region, Ghana. It has a population of about 213,674 (City
population, 2021) and is near the Weija Dam, which the Government
of Ghana created to supply piped water and support fisheries and
irrigation activities. The dam has provided an ideal situation for
schistosomiasis transmission, with early prevalence ranging from 25
to 89.4% in 1991 - 1992 in areas around the dam (20). A 2019 study in
202 pupils found 135 were positive for schistosome eggs (including
both S. mansoni and S. haematobium) in a peri-urban community
along the Weija dam (21). North Tongu district, the second FAST
Package site in Ghana, is in Volta Region. With a population of
110,891 (City Population, 2021), North Tongu is bounded by Lake
Volta to the west, Akatsi south, and Ho Municipal District to the east.
Lake Volta provides water transportation routes, generates electricity
for the Volta River Authority and is a primary resource for fish
farming and irrigation in the region.
Madagascar is an island country in the Indian Ocean off the
coast of East Africa. Madagascar has 114 districts, and is
predominantly populated by people belonging to the Malagasy
ethnolinguistic group. Madagascar has an estimated population of
about 25 million, with more than 60% below the age of 24 years and
32% within 25-54 years (49.3% males and 50.7% females) (22).
About 64% of the Madagascar population are literate.
Morondava District located in the Menabe Region is one of the
FAST Package districts in Madagascar. It is found in the delta of the
Morondava Region with a population of about 150,531. It has a
reported schistosomiasis prevalence rate of 79% and the highest
incidence of HIV in Madagascar. Sakaraha District is in the Atsimo-
Andrefana Region, Madagascar. It has a population of 150,356 and
a schistosomiasis prevalence rate of 82% (22). Mining activities,
including river mining are common in Sakaraha.
Questionnaire and qualitative topic
guide development
The questionnaires and topic guides were designed to explore
the existing sociocultural context, awareness, knowledge, perception
and practices, health-seeking behaviors, and access to preventive
chemotherapy (Praziquantel or PZQ) for schistosomiasis and FGS.
Research instruments were developed based on known influences
found in recent literature on FGS. The in-depth interview, FGD,
and photovoice topic guides were developed based on experience
from a previous FGS qualitative study in Ghana (4,23).
Questionnaires were modified slightly from the baseline at the
end-line, to assess the change in awareness, knowledge,
perception and practices, health-seeking behaviors, and access to
preventive chemotherapy (PZQ) for schistosomiasis and FGS
following the delivery of FGS interventions initiated by the
FAST Package.
Research instruments were developed in English and translated
into French and Malagasy by local and English language specialists.
After that, the local language versions were given to another expert
in the same local and English language to translate the instruments
back into English. This back translation was done to ensure the
accuracy of the translation. The translations were given to a panel of
expert local language speakers of the study location for validation.
The translation exercise ensured adequate comprehension of the
instruments’content and enabled the enumerators to ask the
questions the same way without distorting their original
meanings. To test the understandability of the research tools, the
questionnaire was piloted to a small sample of individuals, and
feedback was used to revise and ensure the final version was clear
and language appropriate.
Data collection
The FAST Package adopted the modified EPI population
proportion sampling frame (24) for the community survey for
baseline and end-line assessments. For the community members’
survey, 30 (clusters) of 14 households per district per country
(n=420 per district at baseline and n=420 at endline) were
identified. The thirty (30) clusters within each district were
selected with probability proportionate to the most recent census
estimate of the community population size by systematic selection
from a list of cumulative population sizes. At the village level, the
enumerator team either selected 14 households (for one cluster)
randomly from an available community list of households or the
enumerator team went to the center of the village, threw a pen onto
the ground, and walked in the direction the pen pointed to in
selecting the first house. If one village has more than one cluster, the
Krentel et al. 10.3389/fitd.2024.1395467
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starting points for each random walk differ. Only one community
member (18 years and above) per household was interviewed.
Enumerators made a list of all eligible household members and
randomly selected one person to participate in the survey. For the
teachers’survey, 5 teachers (18-60 years) were purposively sampled
in each of the thirty clusters/communities selected for the
community-based survey (n=150 teachers per district).
The in-depth interviews (IDI) occurred at the same time as the
surveys in the same selected districts with 4 teachers and 1 district
health director/medical officer per district per country during
baseline and 4 teachers, 1 district health director/medical officer,
8 clinicians and 4 parents per district per country at endline. The
study participants for these in-depth interviews were 18 years and
above and selected using a purposive sampling frame. The focus
group discussions (FGD) were conducted using a purposive
sampling frame with three groups of women of reproductive age
(18-49 years) and one group of men (18-60 years) per district, per
country at baseline and endline. The aim of the qualitative research
was to understand cultural beliefs and practices concerning
schistosomiasis and FGS.
At the endline assessment, photovoice with a group of women
of reproductive age using photography and group dialogue was used
to deepen the understanding of the issues women face with FGS
within their communities. The photovoice approach explored their
feelings, views, and perspectives about schistosomiasis and FGS
using pictures taken of objects or images near the meeting room/
area where the discussion took place. Photos were shared with the
group participants for discussion.
In all study districts, research partners selected and trained
locally based enumerators on the methodology for the survey and
qualitative guides. Quantitative data was collected using the Redcap
platform (Version 10.5.1.).
Data management and analysis
Quantitative data generated through the community and
teachers’surveys were managed through the REDCap platform,
exported to Excel spreadsheet, Statistical Package for Social Sciences
(SPSS) version 26, and STATA 14 readable formats, and analyzed
using descriptive statistics. The results obtained were expressed in
simple percentages, tables, and charts. Chi-square was used to test
for association between categorical variables at 0.05 alpha level.
Item-by-item pre-post comparisons were done by running cross-
tabulations variables pre-vs. post interventions. Multiple logistic
regression was carried out. All analyses were done at a 5% level of
significance and a 95% confidence interval.
For the qualitative data, recorded interviews were transcribed
verbatim in the local language and then translated into English and
French. The researchers read through each transcript, recording
emergent themes in an Excel matrix. NVivo 12 software was used
for coding and analysis of the interview transcripts. The coding
process followed an integrated approach, making it deductive and
inductive. All interviewees were assigned anonymous numbers so
that no identifier could be used to identify respondents to
maintain confidentiality.
Project intervention phase
The FAST Package utilized the results and feedback from the
baseline assessments to inform the interventional phase. The team
engaged appropriate stakeholders at the global, national and district
levels to design, test, implement, and monitor interventions. FAST
Package interventions are described in Figure 2.
Ethics statement
All research activities were covered under the ethical approvals
of Bruyère REB Approval (M16-20-061), University of Ottawa (H-
08-21-7345), University of Health and Allied Sciences Ghana
(UHAS-REC A.5[4] 20-21), Ghana Health Service (GHS-ERC
003/04/21), and Comited’Evaluation Ethique pour la Recherche
Biomedicale, INSPC Madagascar (013/2021-CEER/INSPC).
Results
This section highlights the summary of data collected during the
project and the high-level findings relating to the different
components of the FAST package across the baseline assessments,
interventional phase, monitoring, and endline assessments (Table 1).
Results are described along the four components of the FAST
Package: awareness, prevention of new cases, training of medical
personnel and diagnosis and treatment and the FGS national committee.
Awareness of schistosomiasis and FGS in
the community
As illustrated in Table 2, there is higher awareness about
schistosomiasis amongst community members in both sites,
compared to awareness about FGS. This was consistent across all
rounds of the surveys.
All communities included in the sample are located close to
water sources where schistosomiasis transmission has been ongoing
for many years. As such, participants noted the disease in their
communities during the qualitative interviews, specifically
mentioning the presence of urine in blood.
“We are all aware and have experienced Schisto in this
community. It is because of the river that we use for our
activities.”(FGD, Men, Vome, Ghana)
“Both boys and girls get it. But it is easy to see it in the boys than
in the girls.”(FGD, Men, Tomefa, Ghana)
“My experience with it is that it is more prevalent in the boys
than the girls. For obvious reasons, the boys go and swim more in
the river than the girls, so it is more prevalent in the boys. I have
seen some cases of schistosomiasis in boys in this school.”(IDI,
Male teacher, North Tongu, Ghana)
“I know bilharzia by this very name, and what I know of its
manifestations is that it causes pain in the lower abdomen,
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stomach aches and the end of the urine is blood.”(FGD, female
29-49 years, Morondava, Madagascar)
While awareness of schistosomiasis could be considered high,
some people still were not aware about the disease, despite having
heard about the mass drug administration through schools, as
illustrated in the quote below.
“I have never heard of bilharzia. There has been some sensitization
on the polio vaccine, for example, but I have not heard anything
else except during the distribution of anti-bilharzia drugs to
schools.”(FGD, Men, Morondava, Madagascar)
Compared to schistosomiasis awareness, levels of FGS
awareness were lower in all study sites. In Ghana, levels of FGS
awareness were higher than in Madagascar which may reflect
previous research activities in the country prior to the start of the
FAST Package (25). Some respondents knew of the symptoms of
FGS, as illustrated here.
“In my opinion, the manifestations are not the same, if it’s a little
boy it’s as we mentioned earlier, pain in the lower abdomen and
he urinates blood, but if it’s a girl I thought I already heard that
her vagina was itchy, with sores, plus the presence of a liquid that
runs, and when he was taken to a doctor, he said that it was
bilharzia.”(FGD, female 29-49 years, Morondava, Madagascar)
Despite relatively low awareness about FGS across the community,
women in the study sites were aware of the symptoms caused by
schistosomiasis and FGS. In the FGDs with women of reproductive
health age, photovoice was employed to explore the impact of
suspected FGS felt by women. The findings from these sessions
revealed that the impact of FGS symptoms on women and girls is
stigmatizing and discriminatory.
FIGURE 2
FAST Package interventions.
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For example, in Madagascar, study participants used
dried leaves to explain the stress related to FGS. One of
them stated that “dried leaves are withered and ugly.”Another
woman mentioned that “dried leaves can be relatable to poor
health, vulnerability as well as the shame of showing ourselves
to others”(Photovoice, Women, 29-49 years, Morondava,
Madagascar) (Figure 3).
In Ghana, one study participant used an abandoned building to
explain social exclusion resulting from FGS. She stated explaining
the image in Figure 4:
“As a woman, when you start urinating blood, and you do not treat
it, it comes with a whole lot of complications. An example is infertility,
TABLE 1 Summary of data collected over the lifetime of the FAST Package project.
Ghana Madagascar
Baseline Endline Baseline Endline
Quantitative methods
Community Survey N=869 N=886 N=849 N=846
Male 355(40.9%) 331(37.4%) 377(44.4%) 339(40.1%)
Female 508(58.5%) 552(62.3%) 470(55.4%) 499(59%)
18-30 years 330(38%) 396(44.7%) 424(49.9%) 362(42.8%)
31-43 years 302(34.8%) 295(33.3%) 278(32.7%) 297(35.1%)
44-59 years 237(27.3%) 195(22%) 147(17.3%) 173(20.4%)
Teachers’survey N=313 N=329 N=254 N=285
Male 167(53.4%) 162(49.2%) 109(42.9%) 119(41.8%)
Female 143(45.7%) 167(50.8%) 145(57.1%) 166(58.2%)
18-30 101(32.3%) 92(28%) 103(40.6%) 125(43.9%)
41-43 133(42.5%) 169(51.4%) 120(47.2%) 132(46.3%)
44-59 78(24.9%) 68(20.7%) 31(12.2%) 25(8.8%)
Qualitative methods
Total Total Total Total
In-Depth Interviews (IDI) with Teachers 8 8 8 8
IDI with District Medical Officers or the District Director of
Health Services
2222
Focus Group Discussion (FGD) with Women of Reproductive Age 6 groups 6 groups 6 groups 6 groups
FGD with Men 2 groups 2 groups 2 groups 2 groups
IDI with health care workers –8–8
IDI with parents –8–8
Photovoice FGD with women of reproductive age –4 sessions –3 sessions
*Some missing variables were noted in sociodemographic indicators in the baseline and endline surveys.
TABLE 2 Results from community surveys in both countries.
Ghana Madagascar
Baseline
(n=869)
Endline
(n=882)
Baseline
(n=849)
Endline
(n=844)
Awareness of Schistosomiasis 771 (88.7%) 739 (83.7%)* 685 (80.7%) 751 (88.9%)*
Awareness of FGS 285 (32.8%) 203 (23%)* 57 (6.7%) 70 (8.3%)
Schistosomiasis prevention- taking PZQ
during MDA 102 (11.7%) 197 (22.3%)* 321(37.8%) 437 (51.7%)*
*denotes Chi Square p<0.04.
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and when you are infertile, there is a problem, you would be neglected
like this building, and there wouldn’t be any hope for you.’’
(Photovoice, young women, 19–29 years, North Tongu, Ghana)
Awareness of schistosomiasis and FGS
amongst teachers
Teachers had higher levels of awareness about schistosomiasis
than community members (Table 3) with over 90% of the teachers
surveyed in Ghana and Madagascar reporting that they were aware
of schistosomiasis. This increased in the endline surveys carried out
in both countries.
Regarding knowledge about schistosomiasis prevention, 12.5%
(n=311) and 59% (n=254) in Ghana and Madagascar, respectively,
knew that taking praziquantel during MDA could prevent
schistosomiasis. This increased at endline to 35.7% in Ghana
(n=327) and 66.3% in Madagascar (n=285).
“Schistosomiasis is contracted and transmitted through water; it
enters through pores in the skin and reaches the blood vessel and
ends up reaching the bladders where it lodges so that when the
person urinates, they urinate blood.”(IDI- Male Teacher,
Morondava, Madagascar)
In Ghana, the increased knowledge of FGS among teachers may
be the result of the Schistosomiasis/FGS Educators booklet developed
by the FAST package team in collaboration with NTD programs in
Ghana and Madagascar. The primary target for distribution of the
booklet was teachers who were involved in school-based MDA. The
booklet was co-designed with the national NTD programs in both
countries, the FGS national committee in Ghana and with the health
promotion unit at the Ministry of Health in Madagascar. Over 3150
hard copies of the booklet were distributed within the study districts
and at the national level. The impact of the booklet was detected in
Ghana where the distribution and use of the booklets occurred prior
to the endline surveys. In Madagascar, distribution was delayed due
to various factors resulting in less time in between distribution and
the endline assessment. In Ghana, teachers (n=327) who indicated
the FGS booklet as a source of information about FGS awareness had
3.91 times (OR=3.91; p-value=0.003 and CI= 1.57-9.75) greater odds
of sensitizing people about FGS than those who did not indicate the
booklet. Furthermore, community members (n=882) who were aware
of the FGS booklet were found to have 3.84 times (OR=3.84; p-value
=0.000, CI=2.15-6.84) higher odds of being aware of FGS relative to
those who were not aware of the FGS booklet. One teacher in
Ghana noted:
FIGURE 3
Photovoice from Madagascar.
FIGURE 4
Photovoice from Ghana.
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“I have the FGS booklet. I show the images on it to the school
children. I educate them that this book was brought from Ho and
we are supposed to use it to teach them daily…’’ (IDI, Teacher,
North Tongu, Ghana)
Prevention of new cases of FGS
The FAST Package did not provide preventive chemotherapy to
communities in the study districts. Rather, by working closely with
the national NTD programs, the project team supported awareness
raising activities that promoted uptake of Praziquantel during the
school-based MDA. Due to the constraints brought by the COVID-
19 pandemic, the MDA schedules in both countries were disrupted
during the project timeline (2020-2022). As a result, the intention of
the FAST Package to roll out promotional materials prior to MDA
was not easily realized.
Furthermore, the timing of the MDA in Madagascar occurred
during a period of food insecurity and drought. As children must eat
prior to taking PZQ, this reportedly affected uptake of treatment.
The challenge of taking PZQ in a period of food insecurity is
illustrated by the following quotes:
“The negative side of this medication is that the teacher will not
provide bread. The parents are all in trouble. There is already the
fact of giving tea to the child by the parents at home, so the
children are hungry before taking the medicine, and they faint!
The tea given to him is not enough, because he has not eaten
before.”(FGD Morondava female 29-49 years)
“I have had students who have vomited, after taking the
medicine, they have vomited and felt dizzy, but this is due to
lack of food and not the medicine.”(FGD Morondava female 29-
49 years)
Across all study sites in both rounds of surveys, more male
members of the household were reported to have taken PZQ during
the last MDA round than female members of the household
(Figure 5). The largest difference in Ghana was in the Weija
District endline survey where 90.39% of respondents reported
male members in their household took the MDA within the last
12 months compared to 37.25% of respondents reporting female
household members. In Madagascar, the difference was particularly
notable in Morondava at baseline, 83.15% of participants reported
male household members versus 64.04% of respondents noted
female household members.
Training of healthcare
providers/professionals
One of the objectives ofthe FAST packageapproach is to increase
the capacity of healthcare personnel to prevent, diagnose, treat, refer
suspected FGS cases, record, and integrate FGS into their clinical
practice to improve women’s reproductive health (See Figure 6). To
achieve this aim, the FAST package conducted an FGS online training
for healthcare professional in Anglophone and Francophone
countries in sub-Saharan Africa. The training was led by Bridges to
Development in collaboration with the Geneva Learning Foundation
(TGLF) and was aligned with the FGS core competencies (6). These
core competencies were developed at the start of the FAST Package
project through a virtual interactive workshop conducted by Bridges
to Development and TGLF in close collaboration with the World
Health Organization (WHO) Department of NTDs. The unique
delivery of the FAST Package online training allowed for cross-
border collaboration and peer-to-peer learning for learners. The
training allowed for the participation of a wide variety of learners
from OB/GYNs to community health workers due to the self-
nomination to participate in the training. This variety
demonstrated the range of healthcare professionals that have a role
to play in the diagnosis, treatment, and prevention of FGS. Following
the online training, an in-person training workshop was conducted at
the national level in Ghana and Madagascar to create subject matter
experts (SMEs). Where possible, individuals who had been involved
with the online training were invited to further deepen their
knowledge. In total the FAST Package virtually trained 504 multi-
disciplinary healthcare professionals in more than 24 anglophone and
francophone countries and 262 healthcare providers in a face-to-face
format in both project sites. In addition, the FAST package created 26
FGS Subject Matter Experts in Ghana and 28 SMEs in Madagascar,
comprising obstetricians/gynecologists, doctors, nurses, midwives,
and health information officers.
The baseline and post-training survey analysis for the online
and in-person trainings (Table 4) showed an increase in knowledge
to diagnose and treat FGS cases among those who completed the
course. Regardless of the delivery format of the training, healthcare
TABLE 3 Results from teachers’surveys in both countries*.
Ghana Madagascar
Baseline
(n=311)
Endline
(n=327)
Baseline
(n=254)
Endline
(n=285)
Awareness of Schistosomiasis 291(93.5%) 314 (96.0%) 242 (95.3%) 284 (99.6%)*
Schistosomiasis prevention-Taking PZQ
during MDA 39 (12.5%) 116 (35.5%)* 152 (59%) 189 (66.3%)
Awareness of FGS 63 (20.3%) 221 (67.5%)* 5 (2.0%) 29 (10.1%)*
*denotes Chi Square p<0.04.
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workers expressed their appreciation to learn about FGS, many
stating that they had never heard of the condition, despite having
seen it clinically in their practices. One midwife in Ghana said, ““My
experience of the workshop was wonderful. At the beginning of the
workshop, I was just wondering how in my 29 years of nursing and
midwifery practice, I never heard of FGS and perhaps could have
been a victim without knowing, particularly being a rural dweller or
failed to suspect a client of FGS.”
One key component of the training in both the online and in-
person platforms was the creation of action plans. Participants
created action plans outlining tangible and practical ways to address
FGS within their existing budget and personnel capacity. These
activities included community sensitization, training for colleagues
on FGS among others. A total of 213 action plans were developed
during the online training and 110 action plans during the in-
person training workshops. Participants received feedback on the
FIGURE 6
Process to develop training for healthcare personnel (*denotes
online delivery).
FIGURE 5
Household members reported to have taken schistosomiasis MDA within the last 12 months. Male member of household includes:son/brother/
nephew/male cousin; female member of household includes: daughter/sister/niece/female cousin; multiple responses possible; n refers to the total
number of participants responding to the question.
TABLE 4 Key results of the FGS Online Training.
Online Train-
ing (Anglophone)
Pre-
Test (n=157)
Post-
Test (n=97)
Knowledge to diagnose FGS 31 (19.7%) 92 (94.8%)
Knowledge to treat FGS 33 (21.0%) 91 (93.8%)
Online Training (Francophone) Pre-Test (n=161) Post-Test (n=116)
Knowledge to diagnose FGS 55 (34.1%) 109 (93.9%)
Knowledge to treat FGS 53 (32.9%) 110 (94.8%)
In-person training (Ghana) Pre-Test (n=116) Post-Test (n=113)*
Knowledge to diagnose 34(28.8%) 69 (96.7%)
Knowledge to treat FGS 27(24.1%) 71 (96.9%)
In-person training (Madagascar) Pre-Test (n=76) Post-Test (n=76)
Knowledge to diagnose 33 (43.7%) 73 (96%)
Knowledge to treat FGS 30 (39.7%) 74 (97.3%)
*Some missing values as some health workers in Ghana either did not fully complete or
partially completed the survey questions.
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action plans from their peers, further refining their ideas. Following
the training, learners were connected via social networking tools
that facilitated continued learning and knowledge sharing across
levels of the health system and national boundaries.
Diagnosis and treatment
In Ghana, the national health information platform had an
indicator for FGS in its national health information system
reporting forms. Despite the availability of an indicator, its
introduction was relatively new and the FAST Package training
activities were able to promote its use and definition. In Madagascar,
the closest indicator within the health information system to indicate
possible FGS was hematuria. However, recorded cases would not be
specific on the presence of urogenital schistosomiasis as other diseases
and infections can result in hematuria.
In both Ghana and Madagascar, frontline health personnel in
the selected districts were provided with a project form to capture if
they suspected an FGS case who they referred for treatment.
Following the training activities, 351 cases of suspected FGS were
reported in Ghana and 33 in Madagascar. Tracking the treatment of
these cases was challenging as Praziquantel was not available
through the primary health care centers in either country.
FGS national committee
The FAST Package was supported by the creation of FGS
national committees, funded through support of WHO’s
Expanded Special Program on NTDs (ESPEN). These committees
brought together national level persons who could provide insight
and create opportunities for integration of FGS into government
health programs, like the HIV/AIDS program, family health, school
health, cervical cancer, and national health training institutions.
The committees provided a reach of FAST Package activities
beyond the two study districts. The secretariat of the committee
was situated within the NTD National Program.
The committee in Ghana was active in promoting training on
FGS across other districts where S. haematobium was prevalent. The
committee worked closely with the cervical cancer prevention
program to sensitize FGS recognition. The membership of the
Ghanian FGS committee included representatives from the
clinical care division, public health division (including NTD
Control Program), family health division, Ministry of Education,
and Ministry of Health. About 103 healthcare professionals
(including 26 district directors) across different cadres were
trained by this committee. The committee also participated
actively in developing and reviewing the Schistosomiasis/FGS
educator’s booklet, which was adopted by the Ghana Health
Service and included in the school deworming training material.
The committee in Madagascar secured high level support for its
activities within the Ministry of Health, however due to many
bureaucratic shifts within the government during the project
period, the FGS committee was not able to be implemented.
Discussion
In the FAST Package study districts in Ghana and Madagascar,
FGS was largely unknown amongst surveyed community members,
healthcare professionals and teachers at baseline, despite good levels
of knowledge regarding schistosomiasis. FGS is both a sexual and
reproductive health issue as well as the result of a parasitic infection,
as such, it is misunderstood by community members and often
missed by healthcare professionals. The impact of this neglect is felt
by women and girls who experience FGS symptomsand are unable to
receive a timely diagnosis and appropriate treatment. Addressing
these gaps and their impact on healthcare outcomes requires a
holistic approach rooted in systemic changes at the demand
(individual, community levels) and supply side (health systems level).
The FAST Package used implementation research to pilot a
holistic approach to address FGS in four selected districts in Ghana
and Madagascar. Baseline data informed the development of
tailored interventions, the national FGS committee aided in
scaling up parts of the FAST Package through its partnerships,
and results at all stages of the research were presented to the NTD
programme in the Ministries of Health in both countries. While the
FAST Package was operational for two years (2000-2022) in Ghana
and Madagascar, there were lessons learnt which can be applied to
other countries considering how to address FGS.
Integrating new activities within the health
system takes time
To sustainably address FGS, there must be an integrated
approach within different elements and existing programs across
the health system. This approach is consistent with the pillars of the
WHO NTD 2030 Roadmap and calls from the research community
(9,26–28). The NTD road map calls for integration among NTDs,
mainstreaming into national health systems, coordination with
relevant programs for other diseases such as HIV, child and
maternal health, and strengthening delivery of interventions
through country health systems (14). FGS is an excellent
candidate for integration, as it is a sexual and reproductive health
issue that can be addressed through HIV, HPV programs, family
health, maternal and child health programs, among others and yet
can be prevented through preventive chemotherapy with
Praziquantel delivered through the NTD programme. To help
integration of FGS activities into other programme areas within
the Ministry of Health, the FAST Package leveraged the FGS
National Committee particularly in Ghana. This resulted in
integration of FGS into some HPV activities and health worker
training as well as the provision of a platform to integrate FGS
awareness and training into other scheduled activities.
Incorporating FGS into the health system across multiple levels
requires a long-term, flexible approach which is tailored to the
national context and system. The World Health Organization
Framework for Action titled “Everybody’sBusiness:Strengthening
Health Systems to Improve Health Outcomes”acknowledged the
persistence of health gaps due to health system inadequacies that
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impact the delivery of health services to those in greatest need despite
advancements in interventions and technologies (29,30).
Understanding the strengths and weaknesses of the health system
can help to guide integration. Varying factors that relate to FGS
integration include financing, political will, health workforce,
availability of commodities such as PZQ and education materials,
data collection through the DHIMS, including FGS case definitions.
During the implementation of the FAST Package,we learned that the
process to integrate the Educator’s booklet into the health system in
both countries was different for example, affecting project planning
and timelines. Although the process took longer than planned, it
resulted in a resource that was approved for continued use within the
Ministry of Health’s NTD programme in both countries.
Integrationwithinthehealthsystemcanbeaffectedby
elections, changes to leadership at different levels and delays due
to government bureaucracy. Anticipating these risks needs to be a
part of program planning. Creating awareness about FGS at the
national level and across multiple departments of the Ministry of
Health can help to mitigate these risks. The FGS committee and
senior level FGS champions can help to sustain and promote efforts
to address FGS within the health system.
Reach endemic communities with FGS
messaging during and beyond the annual
NTD MDA campaigns
A low level of awareness of FGS amongst community members
(‘users’of the health system) and providers of FGS-related health
services in highly endemic areas may lead to a lack of both supply and
demand of health services related to FGS diagnosis and management
(31). Mass drug administration (MDA) programs for schistosomiasis
prevention in highly endemic areas, particularly Sub-Saharan Africa,
have increased awareness of schistosomiasis among the populations
at risk and healthcare providers (32,33). However, awareness of FGS
amongst community members remains low (31,34,35). These
findings align with results from the FAST Package in Ghana and
Madagascar, which demonstrated a high level of schistosomiasis
awareness among community members and teachers in Ghana and
Madagascar and a low level of FGS awareness amongst community
members and teachers, particularly at baseline. Low FGS awareness
levels in the communitycan worsen the social inequalities and gender
gaps among the at-risk population (31). This is particularly important
given the gendered variation of risk of schistosomiasis infection
between males and females as a result of their exposure to snail-
infested freshwater bodies.
At the endline assessment, there was no appreciable increase in
awareness of FGS amongst community members in Ghana and
Madagascar. However, findings from the project showed an increase
in awareness of FGS amongst teachers in Ghana and Madagascar. The
increase in awareness of FGS amongst teachers was likely due to the
impact of the FAST Package Educators’booklet. The dissemination of
the FGS Educators’booklet was intended to coincide with MDA
campaigns and be an integral part of education and awareness at the
school and community levels prior to distribution. However, due to
COVID-19, the MDA schedules in both countries were seriously
affected, resulting in discordance between the booklet’s publication
and distribution and the MDA, affecting the reach of community
members in both countries. The value of included FGS as part of
MDA promotion is expected to increase coverage and uptake of
preventive chemotherapy. As demonstrated in other PC-NTD
programs, education and care for associated morbidities increased
community uptake in preventive chemotherapy offered through MDA
(36). As a manifestation of urogenital schistosomiasis, FGS should be
considered as morbidity management for schistosomiasis, with equal
importance to the administration of preventive chemotherapy in
endemic communities.
Increasing community awareness around the risks and impact
of FGS needs ongoing concerted efforts beyond the annual cycle of
NTD MDA programs. Symptoms and chronic effects of FGS
infection occur outside the MDA cycle and in women and
adolescent girls who are no longer included in the school-based
MDA programs. Exposure to snail-infested water will continue
outside of the MDA cycle, especially if water and sanitation
conditions are not improved. Empowering teachers to deliver
education about schistosomiasis and FGS can help to increase
overall awareness in the community throughout the year.
To ensure that awareness and education becomes institutional,
at the health systems leadership and governance level, FGS
awareness should be promoted across existing health programs
(such as sexual and reproductive health and rights (SRHR), HIV,
HPV, and sexually transmitted infections (STI)) and other
government programs as an important gender, human rights, and
sexual and reproductive health issue (2). This will ensure that
activities continue beyond the annual MDA cycle timeline and
involve other sectors in support of the NTD program.
Expand availability of praziquantel beyond
MDA in school-aged children is needed
Preventive chemotherapy with praziquantel can kill the parasite
causing schistosomiasis and prevent infected people from developing
chronic diseases (male and female genital schistosomiasis). In most
countries, MDA programs mainly target school-aged and are provided
through manufacturer donations and international aid in
collaboration with the health ministries in schistosomiasis endemic
regions (37) leaving out a large proportion of the infected population
who are not in school or who are beyond school age. Furthermore,
given the inadequate water and sanitation facilities within
schistosomiasis-endemic communities, re-infection with Schistosoma
parasites can re-occur in between periods of MDA (38,39). The
updated WHO Guideline on control and elimination of human
schistosomiasis suggests that there may be increased benefits
towards elimination when community-wide distribution goes
beyond school aged children to incorporate pre-school aged
children, older adolescents, and adults (40).
The findings from Ghana and Madagascar revealed uneven
uptake of MDA in schools between males and females at baseline
and endline within the last 12 months. In addition, there is evidence
that boys received MDA more than girls in all four study districts.
These findings suggest that the prevalent belief that schistosomiasis
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is a boys’disease may be impacting the uptake with treatment. High
levels of coverage are required to reach the elimination goals for
schistosomiasis and a more tailored approach to MDA is
needed (4).
The timing of MDA needs to consider seasonal availability of
food and water. Households in some communities may not be able
to provide the food necessary prior to MDA with PZQ. If
community members do not understand the importance of MDA
uptake as a preventive measure against the chronic manifestations
of schistosomiasis, they may not see the value in providing
additional food in a period of intense basic need. This will be
increasingly challenging in regions where climate change has
resulted in droughts and periods of famine, in addition to the
impact of climate change on schistosomiasis (41).
According to the proposed framework for assessing gender-
related health systems obligation from an FGS perspective, the
leadership and governance level of the health system should ensure
the expansion of preventative treatment with PZQ beyond schools
to reach adolescents and women. (2).
Innovative training helps to reach a diverse
audience about FGS
There is limited awareness and knowledge of FGS among
healthcare providers, leading to incorrect diagnosis and treatment
(5,6,42). FGS is rarely covered as part of continuing medical
education programs nor is it mentioned in current medical
textbooks (6,7). To reduce gaps in FGS prevention, diagnosis,
and treatment knowledge, the FAST Package developed a training
course that used case-based scenarios and techniques, peer-to-peer
learning, action plan development and implementation. Some of
the elements were based on the experience of and successful
training workshops developed by The Geneva Learning
Foundation and Bridges to Development. The FAST Package FGS
training emphasized syndromic diagnosis of FGS given the resource
constraints in both countries, however colposcope diagnosis was
also included at appropriate levels of care as per FGS core
competencies (6). A unique feature of the online training
program was the method in which participants were identified.
Rather than naming relevant individuals to attend a training or
asking the healthcare system to nominate individuals, participants
self-nominated for the training. As a result, the final cohort of
learners were highly motivated and included representation from
across all levels of the health system (frontline health providers,
district, regional as well as national level personnel), across
countries and across disciplines (general medicine, specialists,
midwifery, nursing, health information officers). This resulted in a
dynamic learning environment for both learners and trainers. For
the in-person training, there was an intent to capitalize on the self-
nominated approach, however it was more challenging given the
need to coordinate travel and attendance in coordination with the
health services. Future training activities would benefit from a
paradigm shift in how learners are identified, away from top-
down selection of participants to include elements of self-
nomination. This approach will ensure that those individuals with
the highest interest, relevant subject matter experience and
motivation are recruited into the training cohort.
The impact of the FGS trainings organized by the FAST Package
continue to be felt at the national and global levels as learners roll
out their action plans in their own contexts. Unfortunately, it was
beyond the remit of the project to capture these ripple effects;
however, certain activities were made known to the FAST Package
team, like the creation of the National FGS Society in Nigeria
(https://fgssofnigeria.com.ng/) which was a direct result of the
online training platform (43). Some FGS SMEs have continued
training healthcare workers through the implementation of their
action plans.
Strong demand for more knowledge and
information on FGS, including integration
of FGS training material into routine health
personnel pre-service training
The FGS online training had a broader reach beyond the FAST
Package implementation countries. The reach helped to increase the
depth and experience of the training for the participants in both
Ghana and Madagascar, providing them with feedback and lived
experiences from professionals working in other countries. During
the online FGS workshops, the FAST Package team observed a far
higher level of interest than expected and a high intrinsic
motivation to develop and implement local solutions. The in-
person SME training workshops in both countries included
individuals who work in national training institutions. The aim of
including these individuals in the SME training was that they would
return to their institutions and consider the inclusion of FGS into
their existing curriculum. In Ghana this included a module on FGS
for continuous professional development in the Ghana College of
Medicine and Physicians, inclusion at the nursing school at the
University of Health and Allied Sciences and at Heritage Christian
University. In Madagascar, nine institutions have included
information on FGS in their training of paramedical personnel
and three (out of six) Faculties of Medicine in Madagascar now
include information on FGS during hospital training in obstetrics
and gynecology. Globally, a reference to aid national training
institutions to develop their own FGS curriculum is needed.
Reporting of FGS through the District
Health Management Information System is
non-existent or newly introduced
Although the FAST Package detected nearly 400 cases of
suspected FGS as a result of its healthcare personnel training,
there was likely under-reporting of cases. In both countries, there
is no FGS case definition currently in use. In addition, there is no
indicator to report FGS or genital schistosomiasis within
Madagascar’s District Health Management Information System
(DHMIS). In Ghana, there is the genital schistosomiasis indicator
on the Ghana DHMIS; however, the awareness of the genital
schistosomiasis indicator is still gathering momentum among
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frontline health care providers who lack the awareness and
knowledge on FGS. The framework for assessing gender-related
health systems’obligations to FGS recommends making available
guidelines for diagnosis and treatment of FGS at the health facilities,
the inclusion of an FGS indicator, and reporting into the Health
Information System (2). To understand the burden of FGS in
endemic areas, accurate and consistent reporting is needed.
Collaboration in between Schistosoma haematobium endemic
countries would help facilitate understanding on what indicators
are in use within the DHMIS, how they are defined and reported.
Regional bodies like WHO ESPEN and Kikundi community of
practice for African program managers can help to transmit these
experiences and learnings in between countries.
Limited availability of PZQ for treating
women and girls outside of the MDA cycle
The regular supply of praziquantel (PZQ) for treating women
and girls with suspected cases of FGS within the community was
challenging in Ghana and Madagascar. The PZQ donations were
primarily for preventive treatment of school-aged children (5-14
years) through MDA, making it difficult for young women and girls
with signs and symptoms of FGS to access treatment at the primary
health care facility level outside of the MDA cycle. There were no
PZQ tablets in health facilities, and the cost of procuring a single
dose of PZQ can be expensive. The WHO policy brief recommends
that adolescent girls and women of reproductive age be provided
with deworming treatment with PZQ for schistosomiasis (40,44).
Advocacy for wider access to PZQ within the health system and the
inclusion of a budget line for FGS as part of the SRHR programs to
procure PZQ and train personnel on FGS prevention, diagnosis,
and treatment is recommended as part of the governance and health
financing health systems building block for FGS (2).
In-country FGS National Advisory
Committee can be incredibly powerful
and dynamic
Through the FAST Package, the NTD Program in Ghana
established a multi and cross-sectoral FGS National Advisory
Committee to increase communication and collaboration about
FGS with the longer-term goal of integrating FGS management into
existing clinical training and care. The FGS National Advisory
Committee created awareness on FGS prevention, diagnosis, and
treatment beyond the FAST Package implementation districts.
When considering the importance of integration and
sustainability of programs, national cross-sectoral committees
provide a platform for discussion and innovative approaches. In
the FAST Package, there were rich exchanges between the NTD
program managers in Ghana and Madagascar as they shared ideas,
challenges, and opportunities with each other. Some of the
challenges of this type of national level committee include the
potential for change in leadership within the NTD program,
bureaucratic barriers and challenges that exist within the system
and the importance of good professional relationships. Ideally, the
FGS National Committee should be a pilot for other NTDs that
require multi-sectoral action to ensure and sustain elimination.
Limitations
The FAST Package project was initiated during the COVID-19
pandemic, launching in July 2020. The associated intermittent
lockdowns, in-country and cross-country restrictions of travel,
and inability to hold face-to-face meetings affected the timeline of
the project’s implementation, including project launch in Ghana
and Madagascar, ethical approvals, baseline data collection,
formation of the National FGS Advisory Committees, the
distribution of the educator’s booklets as well as the delivery of
mass drug administration. In addition to COVID-19, there were
other contextual challenges that included insecurity, climatic events
(drought) and other disease outbreaks during the project period.
Given that the FAST Package project used an implementation
research approach which is inherently grounded in the context in
both countries, this allowed the team to understand some of the
constraints that program personnel at all levels face in the
implementation of schistosomiasis and FGS integration programs.
The aim of the FAST Package approach is a holistic approach to
sustainably address FGS within the health system. It is contingent
on the participation of the health system actors and dependent on
their timelines. Changes at the system level are complex and take
time. Ensuring that FGS is addressed within the health system at all
levels will require patience and perseverance as it will take time.
Furthermore, the engagement of global actors in these changes is
essential as they can provide opportunities for integrated financing,
reporting and action. The FAST Package in Ghana and Madagascar
was limited to two years, as such, we were not able to realize all the
systemic changes we hoped for within the project timeline. We
planned for greater community engagement in the selected districts.
However, at the start of the project, we noted the low levels of FGS
awareness amongst healthcare personnel in all districts and so we
focused more on training and awareness of these key individuals so
that they could respond when demand for FGS services eventually
came from the community.
The FGS national committee in Madagascar was not able to be
fully implemented due to unexpected bureaucratic shifts and hurdles
during the project period. Despite having high level support for the
committee, it was not able to be implemented. This highlights the
challenges and realities of implementing integrated national
committees. Leveraging the present political will present, the FAST
Package team continues to work to implement the committee.
Conclusion
At the time the grant was issued, the FAST Package in Ghana and
Madagascar represented one of the largest single investments focused
on addressing FGS within the healthsystem. Since its inception, there
has been an increase in global attention on FGS and new projects in
Krentel et al. 10.3389/fitd.2024.1395467
Frontiers in Tropical Diseases frontiersin.org14
Sub Saharan Africa. The FAST Package provides a learning
opportunity on the integration of FGS into the health system. It
demonstrates the value of innovative and diverse training platforms;
the importance of local and national FGS champions to integrate FGS
into the health system and pre-service training curriculum; the
importance of consistent and regular awareness on FGS outside of
the annual MDA cycle; the urgent need to ensure the availability of
PZQ at the primary health care centers in endemic areas and; the
need for a systems approach to ensure sustainable integration of FGS
into the health system. The authors view the FAST Package is an
approach. As such, the authors welcome other schistosomiasis
endemic countries and research teams to adapt and implement the
FAST Package as they seek to address FGS.
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Ethics statement
The studies involving humans were approved by The Bruyère
Research Institute (M16-20-061), University of Ottawa (H-08-21-
7345), University of Health and Allied Sciences Ghana (UHAS-REC
A.5[4] 20-21), Ghana Health Service (GHS-ERC 003/04/21), and
Ministère de la Sante Publique, Madagascar (013/2021-CEER/
INSPC). The studies were conducted in accordance with the local
legislation and institutional requirements. The participants
provided their written informed consent to participate in this study.
Author contributions
AK: Conceptualization, Formal analysis, Funding acquisition,
Investigation, Methodology, Project administration, Resources,
Supervision, Writing –original draft, Writing –review & editing.
KA: Data curation, Formal analysis, Investigation, Methodology,
Project administration, Software, Supervision, Validation,
Writing –original draft, Writing –review & editing. MR: Data
curation, Formal analysis, Investigation, Methodology, Project
administration, Supervision, Writing –review & editing. JO:
Resources, Supervision, Validation, Writing –review & editing.
CR: Resources, Supervision, Validation, Writing –review & editing.
FR: Data curation, Formal analysis, Investigation, Methodology,
Project administration, Supervision, Validation, Writing –review &
editing. MD: Data curation, Formal analysis, Investigation, Writing
–review & editing. MI: Data curation, Formal analysis,
Investigation, Software, Writing –review & editing. IU-W: Data
curation, Formal analysis, Investigation, Project administration,
Writing –review & editing. CP: Supervision, Validation, Writing
–review & editing, Resources. MS: Data curation, Formal analysis,
Writing –review & editing. KP: Data curation, Formal analysis,
Writing –review & editing. JJ: Conceptualization, Funding
acquisition, Methodology, Project administration, Resources,
Supervision, Writing –review & editing, Investigation. MG:
Conceptualization, Formal analysis, Funding acquisition,
Methodology, Project administration, Resources, Supervision,
Validation, Writing –review & editing, Investigation.
Funding
The author(s) declare financial support was received for the
research, authorship and publication of this article. The FAST
Package was supported by Grand Challenges Canada. Grand
Challenges Canada is funded by the Government of Canada and
is dedicated to supporting Bold Ideas with Big Impact ®. This work
also received financial support from the Coalition for Operational
Research on Neglected Tropical Diseases (COR-NTD), which is
funded at The Task Force for Global Health primarily by the Bill &
Melinda Gates Foundation (OPP1190754), by UK aid from the
British government, and by the United States Agency for
International Development through its Neglected Tropical
Diseases Program. Under the grant conditions of the Foundation,
a Creative Commons Attribution 4.0 Generic License has already
been assigned to the Author Accepted Manuscript version that
might arise from this submission. Additional funding for the FAST
Package was provided by Merck Global Health Institute, WHO
Expanded Special Project for the Elimination of Neglected Tropical
Diseases, with in kind support from Unlimit Health (formerly the
Schistosomiasis Control Initiative Foundation). The funders had no
role in study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Acknowledgments
The authors wish to thank the communities of Morondava,
Sakaraha, North Tongu and Weija districts and the healthcare
professionals serving them for their participation in the FAST
Package. We also acknowledge the members of the FGS National
Committee in Ghana and thank them for their enthusiasm in
supporting FGS integration. For the online training, we are
grateful to the team at The Geneva Learning Foundation for their
excellent support in the delivery of the first online training for FGS.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated organizations,
or those of the publisher, the editors and the reviewers. Any product
that may be evaluated in this article, or claim that may be made by its
manufacturer, is not guaranteed or endorsed by the publisher.
Krentel et al. 10.3389/fitd.2024.1395467
Frontiers in Tropical Diseases frontiersin.org15
References
1. WHO. Ending the neglect to attain the Sustainable Development Goals : A road
map for neglected tropical diseases 2021–2030 (2023). Available online at: https://www.
who.int/publications-detail-redirect/9789240010352. (Accessed: March 4, 2024)
2. Vlassoff C, Arogundade K, Patel K, Jacobson J, Gyapong M, Krentel A. Improving
the response of health systems to female genital schistosomiasis in endemic countries
through a gender-sensitive human rights-based framework. Diseases. (2022) 10:125.
doi: 10.3390/diseases10040125
3. Ayabina DV, Clark J, Bayley H, Lamberton PHL, Toor J, Hollingsworth TD.
Gender-related differences in prevalence, intensity and associated risk factors of
Schistosoma infections in Africa: A systematic review and meta-analysis. PloS Negl
Trop Dis. (2021) 15:e0009083. doi: 10.1371/journal.pntd.0009083
4. Kukula VA, MacPherson EE, Tsey IH, Stothard JR, Theobald S, Gyapong M. A
major hurdle in the elimination of urogenital schistosomiasis revealed: Identifying key
gaps in knowledge and understanding of female genital schistosomiasis within
communities and local health workers. PloS Negl Tro p Dis. (2019) 13:e0007207.
doi: 10.1371/journal.pntd.0007207
5. Mazigo HD, Samson A, Lambert VJ, Kosia AL, Ngoma DD, Murphy R, et al.
Female genital schistosomiasis is a sexually transmitted disease”: Gaps in healthcare
workers’knowledge about female genital schistosomiasis in Tanzania. PloS Global
Public Health. (2022) 2:e0000059. doi: 10.1371/journal.pgph.0000059
6. Jacobson J, Pantelias A, Williamson M, Kjetland EF, Krentel A, Gyapong M, et al.
Addressing a silent and neglected scourge in sexual and reproductive health in Sub-
Saharan Africa by development of training competencies to improve prevention,
diagnosis, and treatment of female genital schistosomiasis (FGS) for health workers.
Reprod Health. (2022) 19:20. doi: 10.1186/s12978-021-01252-2
7. UNAIDS. No more neglect—Female genital schistosomiasis and HIV —
Integrating sexual and reproductive health interventions to improve women’s lives |
UNAIDS (2019). Available online at: https://www.unaids.org/en/resources/documents/
2019/female_genital_schistosomiasis_and_hiv. (Accessed: March 4, 2024)
8. Gyapong M, Theobald S. The sexual and reproductive health issue you’ve
probably never heard of…. openDemocracy (2015). Available online at: https://www.
opendemocracy.net/en/5050/sexual-and-reproductive-health-issue-youve-probably-
never-hear/. (Accessed: March 4, 2024)
9. Engels D, Hotez PJ, Ducker C, Gyapong M, Bustinduy AL, Secor WE, et al.
Integration of prevention and control measures for female genital schistosomiasis, HIV
and cervical cancer. Bull World Health Organ. (2020) 98:615−624. doi: 10.2471/
BLT.20.252270
10. Brodish PH, Singh K. Association between schistosoma haematobium exposure
and human immunodeficiency virus infection among females in Mozambique. Am J
Trop Med Hyg. (2016) 94:1040−1044. doi: 10.4269/ajtmh.15-0652
11. Downs JA, Dupnik KM, Van Dam GJ, Urassa M, Lutonja P, Kornelis D, et al.
Effects of schistosomiasis on susceptibility to HIV-1 infection and HIV-1 viral load at
HIV-1 seroconversion: A nested case-control study. PloS Negl Trop Dis. (2017) 11:
e0005968. doi: 10.1371/journal.pntd.0005968
12. De Vuyst H, Alemany L, Lacey C, Chibwesha CJ, Sahasrabuddhe V, Banura C,
et al. The burden of human papillomavirus infections and related diseases in Sub-
Saharan Africa. Vaccine. (2013) 31:F32−F46. doi: 10.1016/j.vaccine.2012.07.092
13. Kharsany ABM, Karim QA. HIV infection and AIDS in Sub-Saharan Africa:
current status, challenges and opportunities. Open AIDS J. (2016) 10:34−48.
doi: 10.2174/1874613601610010034
14. WHO. Deworming adolescent girls and women of reproductive age. Policy brief
(2021). Available online at: https://www.who.int/publications-detail-redirect/
9789240037670. (Accessed: March 4, 2024)
15. Krentel A, Steben M. A call to action : ending the neglect of female genital
schistosomiasis. J Obstetrics Gynaecol Canada. (2021) 43:3−4. doi: 10.1016/
j.jogc.2020.11.008
16. Hotez PJ, Harrison W, Fenwick A, Bustinduy AL, Ducker C, Sabina Mbabazi P,
et al. Female genital schistosomiasis and HIV/AIDS: Reversing the neglect of girls and
women. PloS Negl Trop Dis. (2019) 13:e0007025. doi: 10.1371/journal.pntd.0007025
17. Williams CR, Seunik M, Meier BM. Human rights as a framework for
eliminating female genital schistosomiasis. PloS Negl Trop Dis. (2022) 16:e0010165.
doi: 10.1371/journal.pntd.0010165
18. Special Programme for Tropical Diseases Research. TDR Implementation
Research Toolkit (Second Edition). Access and Delivery Partnership. Consulte1 mars
2024, à l’adresse. Available online at: https://adphealth.org/irtoolkit/. (Accessed: March
4, 2024)
19. Leech NL, Onwuegbuzie AJ. A typology of mixed methods research designs.
Qual Quantity. (2009) 43:265−275. doi: 10.1007/s11135-007-9105-3
20. Ampofo JA, Zuta PC. Schistosomiasis in the Weija Lake: a case study of the public
health importance of man-made lakes. Lakes & Reservoirs: Science, Policy and Management
for Sustainable Use. (1995) 1:191–5. doi: 10.1111/j.1440-1770.1995.tb00023.x
21. Anyan WK, Abonie SD, Aboagye-Antwi F, Tettey MD, Nartey LK, Hanington
PC, et al. Concurrent Schistosoma mansoni and Schistosoma haematobium infections
in a peri-urban community along the Weija dam in Ghana: A wake up call for effective
National Control Programme. Acta Tropica. (2019) 199:105116. doi: 10.1016/
j.actatropica.2019.105116
22. Conseil national du recensement de la population et de l’habitation, Ministère de
l’economie et des finances, institut national de la statistique and Cellule centrale
d’execution du recensement. Re
sultats globaux du recensement ge
ne
ral de la
population et de l’habitation de 2018 de Madagascar (RGPH-3). Institut National de
la Statistique. (2020).
23. Kukula VA, Gyapong M, Addei S, TseyIH, MacPherson E, TheobaldS. Experiences
with female genital schistosomiasis: A neglected and misunderstood disease. Liverpool UK:
Countdown Consortium (2019). Available at: https://countdown.lstmed.ac.uk/sites/
default/files/centre/FGS%20in%20Ghana%20-%20FINAL.pdf. (Accessed: March 4, 2024)
24. Henderson RH, Sundaresan T. Cluster sampling to assess immunization
coverage: A review of experience with a simplified sampling method. Bull World
Health Organ. (1982) 60:253−260.
25. Dean L, Ozano K, Thomson R. Stronger together: Evidence for collaborative
action on neglected tropical diseases. Int Health.(2023)15:i1−i5. doi: 10.1093/
inthealth/ihad004
26. Nemungadi TG, Furumele TE, Gugerty MK, Djirmay AG, Naidoo S, Kjetland
EF. Establishing and integrating a female genital schistosomisis control programme
into the existing health care system. Trop Med Infect Dis. (2022) 7:382. doi: 10.3390/
tropicalmed7110382
27. Preston A, Vitolas CT, Kouamin AC, Nadri J, Lavry SL, Dhanani N, et al.
Improved prevention of female genital schistosomiasis: piloting integration of services
into the national health system in Cote d’Ivoire. Front Trop Dis. (2023) 4:1308660.
doi: 10.3389/fitd.2023.1308660
28. Umbelino-Walker I, Wong F, Cassolato M, Pantelias A, Jacobson J, Kalume C.
Integration of female genital schistosomiasis into HIV/sexual and reproductive health and
rights and neglected tropical diseases programmes and services: A scoping review. Sexual
Reprod Health Matters. (2023) 31:2262882. doi: 10.1080/26410397.2023.2262882
29. Stockton DA, Fowler C, Debono D, Travaglia J. World Health Organization
building blocks in rural community health services: An integrative review. Health Sci
Rep. (2021) 4:e254. doi: 10.1002/hsr2.254 (Accessed: March 4, 2024)
30. WHO. Everybody’s business—Strengthening health systems to improve health
outcomes (2007). Available online at: https://www.who.int/publications-detail-
redirect/everybody-s-business—strengthening-health-systems-to-improve-health-
outcomes.
31. Rausche P, Rakotoarivelo RA, Rakotozandrindrainy R, Rakotomalala RS,
Ratefiarisoa S, Rasamoelina T, et al. Awareness and knowledge of female genital
schistosomiasis in a population with high endemicity: A cross-sectional study in
Madagascar. Front Microbiol. (2023) 14:1278974. doi: 10.3389/fmicb.2023.1278974
32. Christinet V, Lazdins-Helds JK, Stothard JR, Reinhard-Rupp J. Female genital
schistosomiasis (FGS): From case reports to a call for concerted action against this
neglected gynaecological disease. Int J Parasitol. (2016) 46:395−404. doi: 10.1016/
j.ijpara.2016.02.006
33. French MD, Evans D, Fleming FM, Secor WE, Biritwum N-K, Brooker SJ, et al.
Schistosomiasis in Africa: Improving strategies for long-term and sustainable morbidity
control. PloS Negl Trop Dis. (2018) 12:e0006484. doi: 10.1371/journal.pntd.0006484
34. Kutz J-M, Rausche P, Rasamoelina T, Ratefiarisoa S, Razafindrakoto R, Klein P,
et al. Female genital schistosomiasis, human papilloma virus infection, and cervical
cancer in rural Madagascar: A cross sectional study. Infect Dis Poverty. (2023) 12:89.
doi: 10.1186/s40249-023-01139-3
35. Schuster A, Randrianasolo BS, Rabozakandraina OO, Ramarokoto CE,
Brønnum D, Feldmeier H. Knowledge, experiences, and practices of women affected
by female genital schistosomiasis in rural Madagascar: A qualitative study on disease
perception, health impairment and social impact. PloS Negl Trop Dis. (2022) 16:
e0010901. doi: 10.1371/journal.pntd.0010901
36. Cantey PT, Rout J, Rao G, Williamson J, Fox LM. Increasing compliance with
mass drug administration programs for lymphatic filariasis in India through education
and lymphedema management programs. PloS Negl Trop Dis. (2010) 4:e728.
doi: 10.1371/journal.pntd.0000728
37. Secor WE. Early lessons from schistosomiasis mass drug administration
programs. F1000Research. (2015) 4:1157. doi: 10.12688/f1000research.6826.1
38. Moses A, Adriko M, Kibwika B, Tukahebwa EM, Faust CL, Lamberton PHL.
Residence time, water contact, and age-driven Schistosoma mansoni infection in
hotspot communities in Uganda. Am J Trop Med Hygiene. (2021) 105:1772−1781.
doi: 10.4269/ajtmh.21-0391
39. Zacharia A, Mushi V, Makene T. A systematic review and meta-analysis on the
rate of human schistosomiasis reinfection. PloS One. (2020) 15:e0243224. doi: 10.1371/
journal.pone.0243224
40. WHO. Schistosomiasis (2023). Available online at: https://www.who.int/news-
room/fact-sheets/detail/schistosomiasis.
41. Adekiya TA, Aruleba RT, Oyinloye BE, Okosun KO, Kappo AP. The effect of
climate change and the snail-schistosome cycle in transmission and bio-control of
schistosomiasis in Sub-Saharan Africa. Int J Environ Res Public Health. (2019) 17:181.
doi: 10.3390/ijerph17010181
Krentel et al. 10.3389/fitd.2024.1395467
Frontiers in Tropical Diseases frontiersin.org16
42. WHO. Female genital schistosomiasis: A pocket atlas for clinical health-care
professionals (2015). Available online at: https://www.who.int/publications-detail-
redirect/9789241509299. (Accessed: March 4, 2024)
43. Global Schistosomiasis Alliance. Female Genital Schistosomiasis Society of
Nigeria : A model for local action. Consulte1 mars 2024, à l’adresse. Available online
at: https://www.eliminateschisto.org/sites/gsa/files/content/attachments/2022-04-27/
Case%20Study%20FGS%20Network.pdf. (Accessed: March 4, 2024)
44. World Health Organization. Deworming adolescent girlsand women of reproductive
age. Policy brief. Consulte29 fevrier 2024, à l’adresse. Available online at: https://www.
who.int/publications-detail-redirect/9789240037670. (Accessed: March 4, 2024)
Krentel et al. 10.3389/fitd.2024.1395467
Frontiers in Tropical Diseases frontiersin.org17
