Background
Malaria is thought to have killed between 150 million and 300 million people worldwide during the twentieth century [
1]. Although the situation has improved in the last two decades, malaria remains one of the leading causes of death and ill-health globally [
2]. In 2019 more than 200 million people were diagnosed with malaria and nearly half a million died, more than 90% of whom lived in sub-Saharan Africa (SSA) [
2]. Interventions such as insecticide-treated nets (ITN) and indoor residual spraying (IRS), combined with improved diagnosis and treatment account for most of the reductions in malaria burden [
3]. Yet these interventions appear to have reached the limit of their efficacy in many regions [
4‐
7]. Achieving further gains and not losing ground in the fight against the disease will require the development of novel and complementary interventions [
8‐
10].
Mosquito modification technologies have garnered a great deal of public interest, particularly in SSA, where their impact is expected to be highest as a tool for malaria control and elimination [
9,
11‐
13]. While experiments with some of these technologies, particularly the Sterile Insect Technique (SIT), go back several decades [
14], significant progress has been made recently in the development and evaluation of novel approaches [
15,
16] such as the Release of Insects carrying a Dominant Lethal genes (RIDL) [
17], gene-drive technologies [
15,
18‐
21], or the release of mosquitoes infected with
Wolbachia bacteria and other endosymbionts [
22‐
24].
These technologies are at different stages of development, and face specific questions from the perspective of communities considering their introduction. One important distinction is between interventions aiming to eliminate the relevant mosquito species (population suppression), and those intended to permanently introduce a novel mosquito strain that will block or interfere with pathogen transmission (population replacement) [
15]. These differences suggest the need for distinct communication strategies, and imply a very different set of expectations on the coexistence between modified mosquitoes and the communities hosting the intervention [
25].
Given the promise attributed to these technologies, their purported high-impact, and the numerous uncertainties that still surround their future deployment, extensive stakeholder engagement is essential in order to identify potential obstacles and concerns in malaria-endemic regions [
15,
26,
27]. Opposition to the release of genetically modified mosquitoes in south-east Asia and the Americas [
28‐
30], and evidence of concerns among stakeholders in Mali [
31], Nigeria [
32] and Tanzania [
33] suggest the importance of proceeding with caution [
26,
27]. Robust social scientific research into how these novel technologies are perceived in areas where they might be deployed is a prerequisite for an effective public engagement strategy [
34].
This study investigated community awareness and perceptions of genetically-modified mosquitoes (GMMs) and their potential for malaria control in south-eastern Tanzanian villages where no research or campaign for the introduction of such technologies is currently underway. To examine how a typical malaria-endemic community might respond to the introduction of GMMs technologies, the study explored the different conceptual frameworks and analogies that communities use to make sense of modified mosquitoes as a tool for malaria control.
Results
Characteristics of study respondents
A total of 506 people participated in this study; 16 community leaders who took part in the two FGD sessions, and 490 community members who responded to the survey. Three of the FGD participants had secondary school education (12 years of formal education), and the rest had primary school education (7 years of formal education).
A detailed description of the survey respondents is provided in Table
1. The mean age was 42.5 years (range: 18–88), and were about equally divided between men and women. A majority of the respondents were married, had primary school education, and reported farming as their main income generating activity (Table
1). The reported average monthly household income was 132,155 Tanzanian shillings (~ 60 USD).
Table 1
Socio-demographic characteristics of the survey respondents
Age (in years) | 18–35 | 186 (37.9%) |
36–55 | 207 (42.3%) |
56–88 | 97 (19.8%) |
Marital status | Married | 321 (65.5%) |
Not married | 82 (16.7%) |
Divorced/separated | 39 (8.0%) |
Widow/widower | 48 (9.8%) |
Highest educational level achieved | No formal education | 43 (8.8%) |
Primary school | 358 (73.0%) |
Secondary school | 68 (13.9%) |
College/university | 21 (4.3%) |
Main income generating activitiesa | Farming | 413 (84.3%) |
Entrepreneurship | 174 (35.5%) |
Fishing | 12 (2.4%) |
Animal husbandry | 23 (4.7%) |
Formal employment | 13 (2.7%) |
Previous surveys in the study area have shown high levels of awareness among residents of these communities about malaria and its transmission by
Anopheles mosquitoes [
5,
45,
46]. In this study, two thirds of the respondents (65.1%, n = 319) believed that rural communities experienced higher burden of malaria, 63.9% (n = 313) believed that poor communities experienced a higher burden of malaria, and 61.3% believed that transmission occurred mostly outdoors. However, when asked about specific details, only 15.3% (n = 75) had a good estimate of current malaria prevalence in the country (as reported in the 2018 Malaria Indicator Survey report [
47]). Half (51.6%, n = 253) of all respondents believed that the country was making good progress in malaria control. 59.6%, (n = 292) believed that it was possible to achieve elimination with the current interventions, but 86.1% (n = 422) of respondents indicated that alternative interventions would be necessary to accelerate elimination efforts.
All survey participants responded that any new technologies for malaria control should be effective, affordable, meet in-country regulations and community preferences, and be safe to people, animals and the environment. When asked about trusted sources of malaria-related information, health researchers and health care workers were ranked higher than government officials or politicians (Table
2).
Table 2
Community members’ levels of trust for sources of information on malaria control interventions (N = 490)
Health researchers | 91.2 | 7.6 | 0.4 | 0.8 |
Health care workers | 91.2 | 8.2 | 0.4 | 0.2 |
Government officials | 84.9 | 12.7 | 1.6 | 0.8 |
Politicians | 55.3 | 26.1 | 9.0 | 9.6 |
Awareness of mosquito modification technologies for malaria control
A vast majority of survey participants (94.3%, n = 462) reported no prior awareness of mosquito modification technologies for malaria control. For the 13 respondents who were aware, the primary sources of information were Ifakara Health Institute staff, and radio or television. Likewise, nearly all participants 97.3% (n = 477) reported no knowledge of how any of these technologies worked. When asked if they thought modified mosquitoes had ever been released in their communities, 83.5% (n = 409) said they did not know and 16.5% (n = 81) said they had not been released.
None of the community leaders who participated in the focus group discussions reported any prior knowledge of mosquito modification technology. They were able to discuss the subject at length and in detail, however, once they were provided with a brief presentation of issue. They often expressed a great deal of fascination over this approach to malaria control, preferring it over other malaria control interventions. Key attributes of the technology mentioned to justify this preference were the improvement of environmental safety (as a result of reducing the use of chemical insecticides), and the little effort the technology appeared to require from local residents (in contrast to other malaria control methods, such as larviciding or home improvements, deemed more labor intensive).
Although three distinct approaches of mosquito modification were presented to FGD participants, participants showed a clear preference for discussing gene drive technologies, and in particular the male-biased sex distorter gene drive that is currently being considered for deployment in several sub-Saharan countries at the moment [
48]. Gene drive technology was preferred because it was seen to require fewer releases of modified mosquitoes compared to the other two, a fact that participants thought would help reduce community skepticism towards the intervention.
“It is better if you do not release mosquitoes all the time. Even if people agree that you release mosquitoes, if you do it a lot they may start asking questions again, then you have to spend a lot of time convincing them. But I like this one that does not kill mosquitoes, but makes them have male babies. With this one you can do it just one time, then it is good.” (Female).
As the above quote suggests, several participants were intrigued by the idea of eliminating mosquitoes by biasing the sex distribution of their offspring, rather than by killing them directly. This was in some cases considered a more humane way of eliminating the mosquitoes.
“I really like the idea of making them have just male babies, because, you see, males do not bite, and without females they cannot have babies. This way even your consciousness is clean, you have not killed them directly, you have just manipulated them and they will eventually die off. This is a very good and very advance technology” (Male).
Framings and analogies used to describe mosquito modification
Although FGD participants were unfamiliar with mosquito modification, they immediately grasped its public health logic by reference to their knowledge of cross-breeding and hybridization. Several participants indicated that the best way to explain this technology to people in the community would be to describe it as a form of ‘kupandikiza’, a term that can be literally translated as transplantation but is commonly used to describe hybrid plants. The term was used, without any prompt from the facilitator, in both FGD sessions. Participants used the example of the hybrid maize seeds that they buy in agricultural shops, which have a relatively higher yield and can better withstand drought than local maize varieties. FGD participants also referred to the technology as ‘kubadilisha mbegu’, the practice of ‘changing seeds.’ The term is generally used to describe the introduction of desirable traits in crop seeds and domestic animals through cross-breeding. Several participants mentioned for example that they often borrow or pay for the use of their neighbours’ male animals in order to get offspring with the desired traits.
“I do it often with my chickens. I don’t have a strong rooster, but my neighbour has a very big one. So I ask my neighbour for her rooster to spend time with my chickens, then I can get its seeds. Everyone does that.” (Female).
“It is very common with pigs. Sometimes there is one person in the village who has a very big boar, so then, if you want to get its seeds you pay that person money so that the boar can mate with your sows. Sometimes you pay money or sometimes you pay him with a litter. But we do that so that we can have the seed for big pigs.” (Male).
Will the modified mosquitoes look and behave differently?
Participants expressed curiosity and concern over the appearance and behaviour of the modified mosquitoes. They wondered, for example, whether or not the mosquitoes would look the same as ‘local’ mosquitoes. Participants drew again an analogy with their experience of selectively-bred animals or hybrid maize, and concluded that the modified mosquitoes would necessarily look different.
“Yes, they always look different. Even when we plant the hybrid maize, it does not look the same as our local maize, it has better yield, and you can tell just by looking that it is different kind of maize.” (Female).
Village leaders were also keen to know whether modified mosquitoes would still bite people, and whether or not current mosquito control tools could or should be applied to them.
I would like to know, if you want those traits to pass to their offspring, will we still need to kill these modified mosquitoes? Will they still bite people? If they bite, people will still want to kill them, and if they do, then it may not work.” (Male).
All mosquitoes are a nuisance; why not just eliminate all of them?
A majority of FGD participants suggested that technologies of mosquito modification should target all mosquitoes, and not just those transmitting malaria. This line of argument was particularly relevant for genetic modification approaches aimed at population replacement, and participants expressed the fear that modified mosquitoes, if they became a feature of the environment, would still be able to carry other pathogens. Additionally, participants stressed the fact that mosquitoes are always a nuisance, regardless of the species; their bites are itchy, painful and cause allergies, so it would be beneficial to just eliminate them altogether. Some participants drew a direct analogy with their experience of jiggers (Tunga penetrans) and lice, which were once prevalent in the region but have been eliminated altogether in their communities. They expected a similar sort of objective should be pursued in the case of mosquitoes.
“We should just eliminate all mosquitoes, the way jiggers were eliminated. In the past there were so many jiggers; as kids we had to go to the hospital to get them removed from our feet. But then something was done and they all disappeared. These days you never hear about them, and the children these days do not even know what jiggers are. I would like that to be the case with mosquitoes, all of them. I would be happy if the future generations do not know anything about mosquitoes, maybe they should only see them in the pictures.” (Male).
FGD participants drew a direct connection between the effectiveness of the intervention and a reduction in the overall density of mosquitoes. They argued that people would only have faith in the merits of the technology if they saw a substantial reduction in nuisance biting. They further noted that most people are unable to distinguish between malaria vector and non-vector mosquito species, and thus would fail to appreciate the impact of the intervention if it was limited to a single species.
“But why would you want the other mosquitoes to remain? For me that is a challenge, that there will still be mosquitoes. People may think that it is not working. The other technologies kill mosquitoes, so then you will know that mosquitoes are not as many. But with this technology there will still be mosquitoes – even if they do not spread malaria, but people will not know that.” (Female).
A few participants, however, did note that mosquitoes also have a place in the ecosystem, and thus supported the idea of eliminating only those responsible for malaria transmission. They pointed out that it would be impossible to eliminate all mosquitoes, because they had never been to or heard of a place where they are completely absent. They further expressed the view that it would be highly important to inform the community that not all mosquitoes would be eliminated, just the ones that spread malaria, so as to prevent mistrust of the technology.
“I do not think there is a need to eliminate all the others if they are not transmitting anything. Remember, there are other birds and other insects that feed on mosquitoes, so it is no use to kill something that is harmless. You know, even in countries that do not have malaria there are still mosquitoes. I know this. So then it is okay to have mosquitoes that do not have malaria. You just need to teach people to differentiate malaria mosquitoes from other mosquitoes so that they know the difference.” (Male).
Importance of engaging and educating community members
All FGD participants stressed the importance of educating and engaging the community in the development of these technologies. They emphasized that this should be done not just once but repeatedly until their level of awareness and knowledge was such that they could participate in any decision to bring the technology into the community.
“It is just very important to make sure that people are well aware of this technology. You have to educate them well. Tell people the benefits of this science, and the risks of continuing to have malaria mosquitoes. I think people should know what can happen if people agree to have these mosquitoes released, and what will happen if they do not. For example, you can talk to people maybe two or three times every month, and do it like that until it becomes a common thing that people talk about. That is when you can come with the modified mosquitoes. It is like that. If you do not do this then it may bring very big problem, and people may even attack you, chase you or embarrass you” (Female).
FGD participants advised that, in order to win the trust of people, researchers would need to come up with means to show people the attributes of this technology, rather than just tell them. Village leaders explained that more efforts are still needed to educate people on different mosquito species, and on how to differentiate between malaria-transmitting and other mosquitoes. Without a degree of familiarity with these issues, it was noted that it would be impossible to convince people that the mosquitoes being released were harmless.
“When you go there with your mosquitoes and tell them that you want to release them, they will ask you if the mosquitoes can harm them, and you will say that these are harmless mosquitoes. They will then ask you to prove it. How will you do that? You will have to find a way of demonstrating to people that these mosquitoes are harmless. If you just tell people that any mosquitoes are harmless you are in for trouble. We all know that all mosquitoes spread diseases, and that all mosquitoes are bad.” (Male).
Discussion
Historically, the release of modified mosquitoes has received a mixed response from the communities hosting these interventions [
49,
50]. Current field research projects on mosquito modification include extensive campaigns of public information and engagement [
30,
51,
52]. It has become abundantly clear that these campaigns must start well in advance of the deployment of the technology, and that they should be preceded by research into the concerns, expectations and interpretive frames that local residents bring to bear on the prospect of making disease control reliant on the introduction of altered mosquitoes into the environment [
13,
27,
53].
This study attempted to explore perceptions of mosquito modification technologies in a region of southern Tanzania where no trials of modified mosquitoes have yet taken place, but where the epidemiology of malaria might in the near future recommend their use. This is a region, furthermore, where many other malaria control interventions have been piloted in the past, and where a significant proportion of the population is familiar with entomological research, thanks to the long-term presence of the Ifakara Health Institute [
5]. This study provides the first social scientific evidence on public perspectives on mosquito modification in Tanzania.
Nearly all community members that responded to the survey reported no knowledge or prior awareness of mosquito modification technologies for malaria control. This is understandable, since no releases have taken place in the country to date, and local and national media have offered very limited coverage of debates on this issue elsewhere in the region. Similar findings have been observed in Mali and Nigeria [
32,
54], for example, as well as in high-income countries such as the USA, where a 2016 survey indicated that 46% of respondents reported no prior information about gene-edited mosquitoes [
55]. The generalized lack of knowledge and awareness made it difficult to assess in detail public perceptions of the technology, at least through a standardized survey questionnaire. FGDs were introduced to allow us to explore mosquito modification technologies in some detail with a select group of local residents, so as to study in depth the specific conceptual frames that might be used to make sense of the technology.
Although all FGD participants had never before heard about mosquito modification, they all expressed a great deal of fascination over this approach to malaria control once the discussions got underway. FGD participants associated the technology to several aspects of their lived experiences, specifically the practice of cross-breeding domestic animals to select for preferred traits, or the adoption of hybrid crop seeds that provide better yield and drought protection. The prospect that similar techniques could be used to eliminate malaria appeared, therefore, intuitively plausible, even before the specific principles of each form of mosquito modification were discussed.
The analogy with forms of biological modification familiar to local residents also shaped their initial consideration of risk, as it allowed them to balance any potential hazards the technology might carry with the promise of a direct benefit. Similar findings have been reported in the US, where support for genetic modification increased once the potential risks and benefits of the technology were communicated to the people [
56]. A study by Widmar et al., for example, indicated that genetic modification was most acceptable when used in human medicine and in disease control [
57]. In this case, participants were relatively supportive of the approach once mosquito modification was contrasted with other malaria control interventions, partly because it was seen as requiring less direct participation from the community, and because it was thought to reduce environmental risks they associated with other interventions (i.e. extensive use of chemicals in IRS, ITNs, or larviciding).
After being presented with several forms of modification, participants expressed the greatest interest in gene drive applications, particularly male-biased sex-distorting alterations. This was due to the low perception of risk associated with male mosquitoes and the high perception of risk associated with female mosquitoes. Previous research in the study site indicate near universal awareness in the community that malaria is transmitted by female
Anopheles mosquitoes, and that male mosquitoes do not transmit any diseases [
38,
58]. The participants also pointed out that the gene drive approach would require fewer and smaller releases compared to other mosquito modification technologies [
15,
18].
FGD participants contemplated the possibility that modified mosquitoes would look or behave differently than local mosquitoes, and sought further clarification on this particular point. These concerns, although expressed mildly in this case, have led to major controversies over the release of modified mosquitoes in the past. Examples include fears that mutations in the mosquito itself, or in the pathogen, could result in higher rates of disease transmission in the future, or that the modification introduced in the mosquito could be transmitted to humans through biting [
32,
33,
59]. It is crucial that these concerns are given careful consideration, and that researchers and sponsors of these technologies are in a position to allay these fears with adequate scientific evidence.
Participants in our FGDs also expressed the concern that eliminating just one mosquito species would not be enough, and would fail to garner sufficient public support for the intervention. This concern can be explained by the fact that people are generally unable to differentiate between malaria vectors and other mosquito species, and that the effectiveness of most other malaria vector control interventions is assessed against a reduction of overall mosquito density. It is estimated that malaria vectors in this region account for less than 10% of the overall mosquito population [
5,
60], and some key vector species, such as
Anopheles funestus, represent a small proportion of anophelines. A technology targeting only a key vector species might be seen as not working if the community experiences little difference in their overall exposure to mosquito nuisance.
Addressing these perceptions and concerns will require a proactive strategy of public outreach. Community engagement in public health research needs to go beyond simply providing the community information or consulting users for their views. An effective program demands building durable partnerships between researchers and the community, eliciting and addressing concerns in terms that resonate locally, and through a process that is embedded within, rather than abstracted from, their everyday lives [
27].
Participants in our study emphasized that it would not be enough to simply raise awareness about these technologies; people needed to be fully engaged in order to make sense of the technology in their specific context. They stressed the need to demonstrate, rather than tell, the safety and effectiveness of the intervention. Similar findings have been observed in studies carried out in Mali and Nigeria, where respondents asked that evidence of the technology’s safety and effectiveness be provided before they could allow it in their settings [
32,
54]. These discussions suggest that education is an iterative process, and that the provision of the facts of how the technology works is only a first step. To truly grasp the public health potential and significance of mosquito modification, communities would need to be able to contextualise these technologies within their everyday life, to translate abstract technical operations into practical concerns.
This study is not without limitations. Only two FGD sessions were conducted, which is a rather small sample size, and the community leaders that participated in the discussions represent a particular segment of the population. Additionally, the study was conducted among communities that have long been associated with public health and entomological research campaigns through Ifakara Health Institute and, therefore, are knowledgeable about malaria transmission and prevention. These limitations to generalizability notwithstanding, the two groups still generated a wealth of qualitative data on the preferred interpretive frames and the most salient concerns that local residents in a rural, malaria-endemic region of Tanzania express in relation to the prospect of using modified mosquitoes as a public health tool. Further studies should be undertaken in communities that may be less familiar with malaria control practices, and to explore in greater depth responses to specific forms of mosquito modification. This study can serve as a baseline from which to develop more granular
investigations of local concerns and perceptions, and upon which to build a robust and effective set of tools for public engagement.
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