INTRODUCTION
Coinfection with malaria and helminths including soil-transmitted helminths (STH) and schistosomiasis are prevalent among preschool and school-age children living in sub-Saharan Africa (SSA), where environmental and host factors contribute to the coexistence of the multiple infections. Malaria and helminth coinfection is associated with anemia, poor physical and cognitive development, and increased mortality.1–3 Current vertical programs recommended by the WHO for the control of malaria and helminths among children have achieved appreciable reductions in the morbidity and mortality associated with the infections. For example, Seasonal Malaria Chemoprevention (SMC), recommended by the WHO in 2012 to prevent malaria infections during high transmission seasons, has provided high protective efficacy against malaria and prevented many malaria cases and deaths.4,5 Seasonal Malaria Chemoprevention is implemented through monthly administration of sulfadoxine-pyrimethamine plus amodiaquine (SP+AQ) to children aged 3 to 59 months living in the Sahel and sub-Sahel regions of Africa, usually through house-to-house visits during the months of the peak malaria transmission season. The remarkable success of SMC has led to the recent WHO recommendation of its extension to other at-risk age groups and highly seasonal malaria transmission settings outside the Sahel region.6
Similarly, WHO recommends integrated approaches to the control and elimination of schistosomiasis and STH through preventive chemotherapy (PC), which comprises periodic administration of anthelminthic medicines (praziquantel for schistosomiasis and albendazole or mebendazole for STH). However, a WHO report on endemic countries across SSAcshowed a substantial reduction in PC coverage for preschool-age children from a coverage of 53.3 million in 2019 to barely 7 million in 2020. In the same year, nearly 71 million school-age children (44.1% coverage) were treated for STH, and approximately 55 million were treated for schistosomiasis (46.6% coverage). This development contributed to the launch of a new neglected tropical diseases (NTD) road map target that reinforced the importance of the paradigm shift from control to elimination of schistosomiasis and STH as public health problems in all endemic countries by 2030.7,8
The overlap in the epidemiology of malaria and helminths has been identified as a potential area to exploit for the development of an integrated control strategy that could help to achieve the WHO targets of eliminating malaria and helminths by 2030.3,9 To our knowledge, no published studies have assessed the feasibility and effectiveness of combining mass drug administration (MDA) for schistosomiasis and STH with SMC, despite the overlap in target populations and potential distribution mechanisms. Furthermore, the few studies10–13 that evaluated the impact of adding anthelminthic drugs to antimalarial medications among school children did not report the acceptability of this approach. Acceptability becomes a crucial issue because of the potential pill burden and the potential of increased adverse drug reactions resulting from co-administration of anthelminthic and SMC drugs. The bitter taste of amodiaquine and praziquantel is known to cause nausea and vomiting when the drugs are used separately.14,15 Occurrence of these symptoms could increase after their combined use, and this may affect the acceptability of the combined treatment approach by children, their parents/caregivers, and those delivering the drugs.
Within the context of a three-arm randomized controlled trial designed to evaluate the feasibility, safety, and effectiveness of integrating helminth control with SMC (ClinicalTrials.gov NCT05354258),16 we have assessed the acceptability, barriers, and enablers of combining the preventive treatment with anthelminthic and SMC drugs among recipients of the drugs, their parents/caregivers, and healthcare providers (malaria and NTD program managers and health workers) in a malaria-helminth coendemic community in Senegal. The findings of this study will support the development of effective approaches to the planning and implementation of an integrated malaria-helminth control approach.
MATERIALS AND METHODS
Study site and context within the trial.
This qualitative study was nested within a trial conducted among preschool and school-age children in the Saraya district of Kedougou region, southeast Senegal. Saraya is ∼800 km from Dakar, the capital city of Senegal. Saraya district, which borders Mali to the east and Guinea to the south, contains 108 villages occupying a land area of 7,803 km2, with an estimated population of 61,756 (2019 population census). More than 70% of the population lives > 5 km from a health facility. The main ethnic groups are Malinke, Fula, Diallonke, and Diakhanke. Farming is the main occupation of Saraya residents. Malaria and helminths are highly endemic in Saraya district.17–20
The current trial was conducted in collaboration with the SMC and NTD programs of the Senegal Ministry of Health and Social Action. Eligible children aged 1 to 14 years were randomized into one of three groups at a ratio of 1:1:1 to determine the safety, feasibility, and tolerability of the anthelminthic and SMC drug coadministration. The first group, which served as a control arm, received vitamin A and zinc on Day 0, followed by SMC drugs on Days 1 through 3; the second group received praziquantel and vitamin A on Day 0, followed by SMC drugs on Days 1 through 3; and the third group received albendazole and praziquantel on Day 0, followed by SMC drugs on Days 1 through 3.16 The anthelminthic and SMC drugs are available in tablet form only. The drugs were administered to the study children according to the WHO recommended dosages, based on their ages and body weights, in the presence of their parents/caregivers. To facilitate administration of the drugs to the children, the tablets were crushed into granulated forms, and a teaspoonful of granulated table sugar was added to the crushed drugs by a trained pharmacist. All child participants were visited at home for 6 consecutive days after coadministration of the study drugs by a trained field assistant to assess the safety and tolerability of the combined drugs. Subsequently, passive surveillance was implemented to monitor any study participants who presented for admission at health facilities in Saraya. In addition, a postintervention survey was conducted 5 months after coadministration of the study medications to assess the effectiveness of the combined treatment approach. Blood, urine, and stool samples were collected from all study participants before and after coadministration of the study drugs.
Participants and study procedures.
This qualitative study was conducted between June and December 2022 among randomly selected parents/caregivers of the child participants in the trial, using a purposive sampling method. Trial participants aged ≥ 10 years were also selected randomly for qualitative interviews. In addition, healthcare workers and trial staff who were part of the implementing team for the delivery of the study drugs were also interviewed. We also conducted in-depth interviews with managers of the SMC and NTD programs of the Senegal Ministry of Health.
Data collection.
The data collection techniques used in this study included structured interviews, in-depth interviews, focus group discussions (FGD) and participant observations. Table 1 illustrates the profile of the study participants who were interviewed in the study. A purpose designed interview guide was used to facilitate the interviews. The interview guide explored the experiences of the parents/caregivers about the trial, their perceptions about the combined use of anthelminthic and SMC drugs, as well as other study procedures including blood, urine, and stool collection from the children, home visits for collection of safety data by trial staff, and the factors that they found encouraging or discouraging about the study. The FGD participants were separated into male and female groups to ensure homogeneity. A ring-form sitting arrangement was adopted. Expression of views was encouraged as each participant was allowed to voice their views freely and each question was discussed exhaustively until the participants raised no new topics. One-on-one interviews with study participants aged ≥ 10 years were conducted using a semistructured topic guide.
Sociodemographic profile of study participants, Saraya district, 2022
| Target group | Number interviewed | Gender | Age range (years) | Site, n | Data collection technique | |
|---|---|---|---|---|---|---|
| Parents/caregivers | 26 |
|
22–50 | Saraya | 4 | Structured interviews and participant observations |
| Khondokhu | 4 | |||||
| Mandakholi | 6 | |||||
| Bembou | 4 | |||||
| Badioula | 4 | |||||
| Dioulafoundou | 4 | |||||
| Study participants aged ≥ 10 years | 10 |
|
10–14 |
|
One-on-one interviews | |
| Health care providers | 4 |
|
28–40 | Saraya Health center | – | In-depth interviews |
| Trial staff | 15 |
|
18–65 | Saraya | 8 | Focus group discussions |
| Bembou | 7 | |||||
| Program managers | 2 |
|
50–55 | SMC and NTD Programs, Ministry of Health and Social Action | – | In-depth interviews |
The trial staff and Saraya health facility staff were also interviewed. The health facility staff were purposively selected and included the medical director of the Saraya health center, a medical doctor at the center, a nurse, and a member of pharmacy staff. Two members of the SMC and NTD programs were also interviewed using a topic guide that included the following themes: 1) perceptions about the integrated delivery of anthelminthic and SMC drugs to children; 2) the feasibility of implementing an anthelminthic-SMC program by a joint team of SMC and NTD program officers; 3) adaptations to working practices that would be required to implement the integrated antihelminthic-SMC program, if it becomes a policy; and 4) recommendations on factors that may facilitate effective implementation of the integrated approach.
The interviews were conducted in French or in any of the local languages preferred by the study participants by the project’s social scientist (Am. D.) and notes on verbal and nonverbal communications were taken by a trained research assistant. Each interview lasted for ∼45 to 60 minutes. All interviews were digitally recorded and transcribed into English. All field notes were coded to maintain the confidentiality of participants. For quality assurance, translations and transcriptions were verified by an independent social scientist who is a native speaker of a Senegalese language and who also speaks English and French.
Data analysis.
The first step in coding the data collected from the interviews was to transcribe the interviews into a written format. This was done manually. After this, we read through the transcripts several times to become familiar with the data and identify potential codes. We identified relevant themes by using a combination of underpinning issues in the interview guides that formed the basis of the research questions and issues that emerged during the interviews. Subsequently, we developed a codebook that outlined the codes and categories that we used to analyze the data. Two members of our team (Am. D. and Ad. D.) coded the data and used NVivo software version 12.0 (QSR International, Burlington, MA), to manage the data and apply the codes. The two researchers who coded the data met regularly to discuss their coding decisions and resolve any discrepancies. Unresolved disagreements by the two researchers were resolved after discussions with a third independent researcher (N. M. S.). As the coding process progressed, the two researchers refined the codebook and added new codes or categories, based on the emerging themes in the data. The coded data were analyzed by using the emerging themes and patterns in the data. This involved creating visualizations such as word clouds to identify similarities between common themes. We triangulated common themes arising from the interviews and included verbatim quotes of the study participants to buttress certain views expressed in the course of the interviews.
RESULTS
Fifty-seven study participants comprising 26 parents/caregivers, 10 study children aged ≥ 10 years, 15 trial staff, four healthcare providers, and two managers from the Senegal Ministry of Health were interviewed. Thirty-eight of the participants (66.7%) were male and 19 were female (33.3%). Their ages ranged from 10 to 65 years (Table 1). The safety data obtained from the active and passive surveillance of participants after coadministration of the study drugs will be published in a separate paper. For this qualitative study, four main themes were identified from the interviews relating to the acceptability, enablers, barriers, and recommendations for implementation of an integrated anthelminthic-SMC program.
Perception and experiences about combining drugs against malaria and helminths.
Perception about the combination of drugs for treatment malaria and helminths.
But we can only be satisfied. Because every year our children fall ill with malaria and stomach aches because of worms so if we are given medicine to treat these two diseases, we must take advantage of it. (PC1, Dioulafoundou, parent/caregiver)
You know we are in a border area and as each rainy season approaches, malaria and worms begin to set in. The swelling of the belly of the child are due to the worms, therefore the medicines are very important for us. (PC2, Khondokhu, parent/caregiver)
Children are in contact with nature eh, here they are everywhere, they wade through stagnant water during wet season. Here, at the backwater, that’s where they go to bathe or swim, so all of this can give them worm diseases. Malaria too, with the mosquitoes that develop in these places where children frequently go. So combining the drugs for malaria and worms for the children can really give a convincing result for better health of these children. (PC4, Bembou, parent/caregiver).
It’s a feeling of satisfaction and a bit of worry because I’m like, “Is this going to continue?” They can get us used to this program this year, and later let us down, that’s my concern, but otherwise it’s a feeling of satisfaction and it must also be said that I felt sorry for some children to see them take many drugs at the same time, but I believed it was for their good. (PC7, Bembou, parent/caregiver)
Yes the feeling that I really had that moved me a lot because not only does it contribute to the good health of my children and it is a way of fighting against these diseases that we do not know, but which ravage the rural area especially in the rainy season. In any case, personally, I find this very important and it’s a feeling of satisfaction that I have because I tell myself that maybe I have good luck, I don’t know if it’s in all over Senegal. (PC9 Dioulafoundou, parent/caregiver)
As CK said, we had a feeling of pride because before, we saw a lot of child deaths, so today it’s a pride to see them taking the drugs for their improved health from malaria and worms. (MA1, Saraya, trial staff)
The feeling I had was fulfillment and satisfaction because, in some way, it contributed to the development of my locality. Since these diseases can lead to several deaths, so if we participate in eradicating them, it is a source of pride for us. Seeing the children taking the medicine also reassures us that they are not going to get malaria or worms. (MA3, Bembou, trial staff)
We know that these are drugs that we are used to giving and each of these drugs cause certain side effects; so I had a little concern about the combination of these drugs and about the reaction in the children’s bodies. It was a feeling of a little worry that drove me, but still after the administration, I saw that there was really nothing to be afraid of. So, I feel a great pleasure to be part of this study. Especially since at the very beginning we were called to give an update on the situation of the malaria and worms in general, and to tell us that this year they intend to combine the drug campaigns of NTD and SMC. (HCP 1, Saraya, health facility staff)
My pharmacy colleagues prepared the dosages of each drug according to a child’s age or weight. It’s across age groups; for each child we administered the dose that goes with it. Like, for example, 3-year-olds and 10-year-olds cannot have the same dosage. We adapted the drugs and put them in sachets, which we gave to the medication administration team. (HCP 4, Saraya, health facility staff)
Experiences after coadministration of anthelminthic and SMC drugs.
I am happy, I also had strong confidence that my child will be protected from these diseases. But there were side effects as the child slept all day after taking the medicine, he also had mild fever but these side effects don’t last long, and that’s normal too.
How long did they last? (Investigator)
Only 24 hours, now he is fine.
Why do you say side effects are normal? (Investigator)
It’s normal because the drugs are not the same if each one does its job, the child must feel it in his body. (PC3, Bembou, parent/caregiver)
Yes, I noticed that one of my children had mild diarrhea, otherwise they remain calm all day, it even looks like they are sick. But the side effects did not last long, now they are doing very well. (PC5, Dioulafoundou, parent/caregiver)
And they gave out a health book telling us that if our kids get sick after the child took the medications, you take them to the health center with the book. They told us that if you go to the hospital, you’re not going to pay anything for the drugs, it’s them who will pay for the drugs. (PC6, Badioula, parent/caregiver)
It’s really the biscuits and drinks that made the job easier and even the children who didn’t take the medication asked their parents why they didn’t receive it like their siblings who took it. That’s really what made the job easier. (PC8, Khondokhou, parent/caregiver)
I will rather talk about what made the job easier. That is, the cookies on the days that we took with us, it made the job a lot easier. When the children saw that their siblings were taking the medicine and then received biscuits, they too came to take it”. (MA5, Saraya, trial staff)
The goal was for the children to be able to have something in the stomach before taking the medicine. But we found it to be a motivator for some who saw these snacks even though it was not included in the study, there were children who wanted to be given the drug just to get the snacks and drinks. (HCP2, Saraya, health facility staff)
As soon as the health workers came to our household, I gathered the children concerned and I saw the health workers were grinding the drugs in a small mortal and giving them to the children. This made it easier for the children to take medicine in addition to the snacks given to the children, this motivates the children to take because they have taken the juices and the snacks. (PC10, Dioulafoundou, parent/caregiver)
Enablers of acceptability of combined medications.
Having established the acceptability of the integrated malaria–helminth treatment approach by the users, we explored further factors that might have contributed to the positive feedback. These included the following.
Perceived effectiveness of SMC.
I witnessed a fact in my household, my brother refused to administer the malaria drugs to his children. I didn’t know initially that he did this because I was in another area. A few days later, one of his daughters fell ill with malaria, we took her to the health center and was referred to Kédougou regional hospital but she eventually died. That’s why I say the district needs to take action on parents who withhold drugs from their children. (MA7, Bembou, trial staff)
But every year we do prevention against malaria and the children who take their malaria medicine regularly have not had the difficulty of contracting malaria during the wet season, as we understand the difference between the children who have taken the medicine and the children who did not take the drug. It is useful for children because the difference is that these children, as I said, do not have malaria unlike the others who had not taken it. (PC10, Mandakholi, parent/caregiver)
Because we understood the usefulness of SMC drugs in successfully rolling back malaria. We understood, we saw the results. The same thing will happen for this new approach. (PC13, Dioulafoundou, parent/caregiver)
I accepted because I saw the benefits of the SMC malaria campaign. I agreed because I believe the benefits of this combined treatment will be successful like that of SMC, and I don’t want my kids to get sick again because of malaria and worms. (PC16, Badioula, parent/caregiver)
Trust in government health programs.
You know, the government and the population is like the father of a family and his children. A father never endangers his own children, he protects them. So, I believe that if the government gives drugs to the population, it is for their good. The government cannot move health workers and investigators from Dakar to Kédougou to give the wrong drugs to the population. In addition, each year, the government gives us treated mosquito bednets to fight against malaria, so if they give us this medicine, I think it is to reinforce the prevention measures. (PC14, Dioulafoundou, parent/caregiver)
If it was another project different from the government project, I would be afraid and worried about the things they give to our children, but as it is the government which is at the origin of this project so that our children can be prevented from malaria and worms, so I will make sure to reciprocate their kind gesture. (PC17, Saraya, parent/caregiver)
Perception on feasibility of the drug combination.
The idea of combining campaigns for the same target population seems to me to be very efficient, in order not only to save financial resources but also resources in terms of time for the organization of these campaigns and which nevertheless allows better integration of activities at the level of the Ministry of Health. (PM1, program manager)
What we find interesting in this combination is the fact of maximizing synergies, especially since we are working on the same target population, and we are the same actors, operating in the same health system. So, it’s important that we are moving towards this integration as it will allow us to be much more time-efficient, ensure better cost-efficiency in the delivery of the intervention especially at the operational level. It will also reduce the workload of the service providers. (PM2, program manager)
Apart from these campaigns, there are other campaigns that are taking place throughout the year; an example is the expanded immunization program, there are so many other campaigns that are carried out, so if we reduce the number of campaigns by integrating them, that would certainly allow for better acceptability. (HCP4, Saraya, health facility staff)
In order not to repeat myself, I can say that it is the fact of combining the drugs. At the strategic level, having better efficiency is beneficial. The two programs are in the same direction, and we do not have the resources for several campaigns. Especially since the campaigns are done with the same actors with the same target populations. (PM2, program manager).
Barriers to acceptability of combined treatment approach.
The parents/caregivers, trial staff, and healthcare providers provided insights on the challenges they encountered when delivering the integrated anthelminthic-SMC drugs to the children. These perspectives are highlighted under the following headings.
Reluctance/refusal by children.
We encountered a lot of difficulty, especially when we went to a house and we can’t find the child concerned, in which case we have to leave and come back because we don’t leave the medicines with the mothers, because it is not sure that they will administer the drugs to the children, which is why sometimes we stay in the field until 11 pm. (MA13, Bembou, trial staff)
I remember that, because I had a child, a boy who refused to allow these people to take his stool.
How old was the child? (Investigator)
He is 13 years old today, I believe.
Why do you think he refused? (Investigator)
The first day they came to my house to take his stools, at the time I had gone to the farm. But when I arrived, his mother told me that. I asked him why he refused, and he told me that it was a woman who had wanted to take his stool. So I asked the staff to come back because they were still here in the village and I personally took the stool and I gave it to a gentleman.
So, if I understand correctly, it’s the fact that it’s a woman that the boy refused?” (Investigator)
For the boys it must be men and for the women too because they are ashamed to see a woman take their stool like that, it bothers them. (PC22, Khondokhu, parent/caregiver)
The first day that we started giving the drugs to the children, we had problems with them, because the drugs are bitter. Some take it straight, but for others you have to pound the medicine to give it to them. The drug like praziquantel is a bit big. Now I don’t know what to do, but I think we will have to try to see another alternative, it can be the same tablet, but it will have to be reduced in size. And also, if it’s possible to do it with a little sugar, so swallowing it will be much easier. (MA6, Badioula, trial staff)
Recommendations.
Parents/caregivers.
The problem with the medicine is the bitter taste. This is what scares the children. We would have preferred it to be easy to take like paracetamol. Because even this 4-year-old child who is there, when I give him the paracetamol, he takes it without difficulty. So, I would have liked that the drugs we give to the children didn’t have a bitter taste. (PC24, Badioula, parent/caregiver)
If they really can change the taste and also the smell, that would be good; because the taste and smell of some of the drugs are problems to the children. That’s what makes children vomit. (PC21, Dioulafoundou, parent/caregiver)
Trial staff, healthcare providers, and program managers.
The recommendation is to improve the taste of the drugs as well as the smell if possible so that these drugs will be much easier to take and absorb. (MA8, Saraya, trial staff)
It is important during the organization of these campaigns to make available to health structures the necessary means to take charge correctly, and in communication to inform the populations, because the principle of medicine is to do no harm: if we give drugs that are not, and which have side effects, we must not make the parents bear the burden and therefore, we must take steps so that the local health authorities, that whether regional, whether hospital, district or health post level, can have the means to take charge of these cases in case side effects may occur. (PM1, program manager)
In any campaign there are refusals that are always recorded; the solution is to organize during these campaigns management committees for cases of refusal to do the advocacy, and also to guarantee to these populations the safety of what we are doing and once they are convinced, I believe they will be able to adopt and agree to take these drugs. (HCP3, Saraya, healthcare provider)
Use all possible channels, currently social networks are very popular with this age group, we have TikTok, we have Facebook, we have all these current tools. I think we will have to adapt the communication to this population through social media and similar networks because young people no longer listen to the radio, or watch local TV stations like before. We can also reach them through their associations, through WhatsApp groups and others to ensure that there is a clear message that can be digested by these young people. (PM2, program manager).
Everything will depend on the results of this study and the different aspects that I have talked about because the overall advantage of this strategy is to save time and money to organize the two separate campaigns because the Ministry of Health is used to organizing these two campaigns. If the results of the final evaluation shows that there is efficacy and safety in the administration of these combined drugs, why would we not make recommendations in this direction? (PM2, program manager)
First you have to disseminate the findings of this study because all things you have gathered in this study needs to be shared with all the players. The different actors need to discuss together to find a solution, and move towards this combination of treatment, especially in areas with high prevalence. More importantly, we know that we have to carry out several interventions, and we are all convinced of the benefits of integration. We have even set up a pilot project to integrate NTD with the other existing platforms in the district of Koungheul. So to ensure the sustainability of our interventions, we have to move towards integration. (PM1, program manager)
DISCUSSION
Senegal has been implementing SMC and MDA for STH and schistosomiasis as separate vertical mono-disease control programs since 2008 and 2009, respectively. Seasonal Malaria Chemoprevention was first evaluated in Senegal in 2008 before its eventual adoption by the WHO for implementation across the Sahel region in 2012.21 The sustained implementation of these two programs has contributed to the reduction of the burden of malaria and STH in Senegal and moved the country to the pre-elimination stage for the two diseases.22,23 In line with the global agenda of eliminating malaria and some NTDs by 2030,24 we conducted this study to assess the provider and user acceptability of an integrated control treatment of malaria and helminths.
Our findings showed that coadministration of anthelminthic and SMC drugs was acceptable to the children, their parents/caregivers, and the implementing team. These findings are consistent with the results of similar studies that have assessed the acceptability of antimalarial25,26 or anthelminthic medications.27,28 Although there were concerns about the unpleasant taste of two key medications (amodiaquine for SMC and praziquantel for schistosomiasis), this did not have a negative impact on the overall acceptance of the integrated treatment approach. This may be due in part to the pragmatic approach adopted in this study to transform the drugs into granulated form by trained pharmacists. The addition of granulated table sugar to the granulated medicines also improved the taste. Sweetening agents such as sucrose are frequently added to pharmaceutical dosage formulations to mask the bitter taste of partially dissolved drugs and to improve palatability in general.29 This method was adopted because of the relative availability of table sugar in the resource-limited setting where the study was conducted. It is hoped that the manufacture of flavored pediatric formulations of amodiaquine and praziquantel will address this concern.
All study participants raised concerns about the side effects associated with the bitter taste of amodiaquine and praziquantel, which led to severe nausea and vomiting in a minority of children. Previous studies have documented the increased incidence of these adverse events with amodiaquine15,30 and praziquantel.31,32 Accurate dosing of age-appropriate, pediatric-friendly formulations is needed to reduce the incidence of these adverse events and improve the palatability of the drugs.31,33
Trust and confidence in government-sponsored health programs came out strongly as the major factor that influenced the acceptability of the integrated malaria–helminth preventive approach deployed in this study. A high level of trust in government and health institutions has been reported in many studies to correlate with high uptake of interventions and improved health-seeking behaviors.34,35 Nevertheless, findings from our studies showed that many of the parents/caregivers believed that the study was specifically developed for the care of their children, a concept described as “therapeutic misconception.”36,37 This might be due to the involvement of government staff who were known in the community to be responsible for the implementation of SMC and MDA for STH and schistosomiasis. This study was developed and implemented in collaboration with the Ministry of Health, and this strengthened its acceptance within the study community. However, when similar collaborative studies between researchers and the Ministry of Health are undertaken in the future, it is important that the expectations of the study population are not raised inappropriately by stressing that the intervention is only at an experimental stage.38 Similarly, snacks were provided to the children as a part of the research implementation to ensure that the study medications were not taken on empty stomach because this could exacerbate the drug–drug interactions between praziquantel and amodiaquine.39,40 Although snacks are not routinely provided in real-life situation during programmatic implementation, children are usually encouraged to eat before taking the medications. This may affect acceptability, uptake, and scalability of the integrated treatment approach.
Refusal and/or rejection of the combined drugs was reported among children who were in the 10- to 14-year age group. On exploration of the factors driving this behavior, it was discovered that peer influence and lack of sensitivity to adolescent sexuality played a significant role. Studies have reported similar findings on how normative beliefs and the behavioral influence of the interactions among peers have hindered young people from utilizing health services because of the fear of stigmatization and gossip.41,42 To overcome this challenge, culturally appropriate and gender-sensitive approaches should be adopted for the administration of the medications and collection of biological samples such as urine or stool from adolescent participants. Also, given their unique physiological changes, specific barriers affecting the adolescents’ acceptability and uptake of the integrated treatment approach should be addressed by involving the adolescents in co-creation and implementation of tailored health and education services that reflect their developmental stage and unmet needs.43
The program managers and healthcare workers provided encouraging insights on the feasibility of a harmonious integration of SMC and MDA for STH and schistosomiasis control. This submission was probably driven by the perceived benefits of cost-cutting and improved efficiency in operational planning and implementation of an integrated control program for malaria and helminths. Although these efforts will involve national and international harmonization and coordination of the activities of partnerships devoted to control or elimination of the two major diseases,44 it is imperative to embrace the increasingly recognized strategy of integration of SMC and MDA for STH and schistosomiasis control into a broader health systems to optimize system effectiveness and cost-effectiveness, particularly in health systems with limited human resources, as frequently found in SSA. The integration also has the potential to accelerate progress toward universal health coverage and advancing the 2030 agenda.45
Our study had a few limitations. The opinions and views expressed by participants in this study were shaped largely by their sentiments on the effectiveness of SMC program in the community and in Senegal as a whole. A key challenge arose in separating the participants’ opinions about the integrated anthelminthic–SMC approach from the component of the SMC intervention because the two were closely linked in this study. Given that the study participants had not experienced an integrated malaria–helminth treatment approach before this study implementation, it was also difficult to clearly separate their views on the integrated approach from similar MDA campaigns that took place previously in the community. Also, a preponderance of male participants in this study might have reduced the information on the lived experiences of mothers who usually played the socially ascribed roles of primary caregivers in most African communities. Nevertheless, our approach of using different interviewing techniques helped to minimize the response bias that might have undermined the findings of this study.
In conclusion, we report the findings of the first study that has explored the providers and caregivers’ acceptability of an integrated malaria–helminth treatment approach within the context of a clinical trial in Senegal. Overall, the approach was well accepted by the study participants, but concerns about the taste and smell of amodiaquine and praziquantel need to be addressed to optimize the uptake of the integrated control program. Also, culturally appropriate strategies need to be put in place to cater for the inclusion of children aged 10 to 14 years if the integrated malaria–helminth control program is to become an international policy.
ACKNOWLEDGMENTS
We appreciate Drs. Babacar Gueye, Doudou Sene, Ndeye M’backé Kane and Boubacar Diop and the entire management at the Senegal National Malaria Control Programme, NTD Control Programme, SMC Programme, and the Ministry of Health and Social Action for supporting the implementation of this study. We also thank the Medical Director and staff of Saraya Health Centres as well as all the child participants and their parents/caregivers.
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