Community Engagement and Social Assessment for Wolbachia-Based Suppression of Natural Populations of Aedes aegypti: The Mexican Experience

Abstract

The Wolbachia-based approach is under evaluation as a control strategy against Aedes aegypti in Mexico. From 2017 to 2019, we performed a pilot study to evaluate an open-field mass-release of wAlbB-infected Ae. aegypti male mosquitoes, as part of an integrated vector management (IVM) plan led by the Ministry of Health in Mexico to suppress natural populations of Ae. aegypti in southern Mexico. Community engagement and social evaluation were part of the key activities conducted. Overall, results showed the positive benefits of this Wolbachia-based method in the reduction of Aedes mosquitoes (90%). Mosquito’s nuisance at bedtime and the increasing circulation of mosquitoes during the releasing days were reported as the negative perceptions of this method. Importantly, participants understood the difference between wild mosquitoes and those released as part of the project, as well as the importance of the IVM. A significant number of the population accepted and supported the project, and feedback was given to improve future mosquito-releasing activities. The social license was a key factor in the success of the intervention and should be part of innovative paradigms for mosquito-vector control strategies involving community engagement. We outline the Mexican experience of community engagement and social assessment in implementing a Wolbachia-based strategy.

1. Introduction

Mosquito-borne diseases remain as one of the major challenges for public health and vector control programs at global and local levels. Up-to-date, there is not a 100% effective vaccine or therapy for dengue, chikungunya, or Zika virus. Hence, traditional mosquito-vector control strategies are among the most common ways to combat these diseases, with proven efficacy [1]. Integrated vector management has been the approach recommended by the World Health Organization [2, 3] to reinforce the vector control programs.

As a result of new biotechnologies for pest control, innovative approaches have been developed for the suppression and/or replacement of mosquito populations. The “rear and releases” is the new change of paradigm in this agenda and social assessment must be a key aspect to consider. A novel strategy to suppress vector populations based on the endosymbiotic bacterium Wolbachia pipientis is a promising complementary strategy that potentially reduces mosquito populations and the risk of mosquito-borne disease transmission [3, 4, 5, 6, 7, 8, 9, 10, 11, 12]. This approach known as the incompatible insect technique (IIT), consists of the release of male mosquitoes infected with maternally inhered Wolbachia. The mating between Wolbachia-infected males and urban/wild-type female mosquitoes in the environment (not infected with Wolbachia) produced non-viable eggs due to a phenomenon called cytoplasmic incompatibility (CI) [4]. However, IIT approaches can combine additional measures, such as the sterile insect technique (SIT) to minimize the unintentional release of fertile Wolbachia-infected female mosquitoes (IIT-SIT approach) (Figure 1) [7, 8, 9]. In this low-dose irradiation is used to sterilize residual pupae females after the sex sorting process, thus preventing the stable establishment of field populations derived from released Wolbachia-infected males [6]. The IIT-SIT approach to suppress Ae. aegypti populations have been tested in two recent successful pilot trials in Thailand [10] and Mexico [13] and Ae. albopictus in China [11]. Furthermore, the circulation of Wolbachia strains in native populations of Ae. albopictus have been already identified in the southern region of Mexico [13, 14].

Figure 1.

The combined IIT-SIT approach is depicted schematically: (A) The four types of possible crosses between wild/urban Aedes aegypti mosquitos and Wolbachia-infected Ae. aegypti mosquitos; and (B) Irradiation of residual Wolbachia-infected females (SIT) to prevent them from reproducing in the wild; mass-production, irradiation, and release of Wolbachia-infected males with residual females, as well as mating crosses with wild/urban populations.

Currently, the Wolbachia-based approach that combines both incompatible and sterile insect techniques (IIT-SIT) is under evaluation as a control strategy against Ae. aegypti in Mexico. From 2017 to 2019 a pilot study was performed to evaluate an open-field mass-release of wAlbB-infected Ae. aegypti males (Wolbachia strain wAlbB from Ae. albopictus [donor host] and successfully established in Ae. aegypti [novel host]), as part of an integrated vector management (IVM) plan led by the Ministry of Health in a semi-urban community called San Pedro Chimay, Yucatan, Mexico, with the collaboration of the autonomous university of Yucatan, to suppress natural populations of Ae. aegypti in southern Mexico [12]. In this pilot study, a protocol for the implementation of a Wolbachia-based biocontrol aiming to suppress Ae. aegypti mosquito population was designed. At first, anthropological research seeking community engagement and cultural sensitization was conducted, followed by an entomological baseline survey. Secondly, the Ministry of Health carried out an attack phase with vector control routines followed by a suppression phase, including male-mosquito releasing activities and the social assessment of the entire project [12].

For the pilot study, community engagement and social evaluation were part of the key activities conducted [15, 16]. Throughout the suppression phase, we observed significant reductions in the adult females collected at the release site in comparison to control sites, with the greatest effect observed on the number of indoor Ae. aegypti females collected per house (90% of reduction efficacy) [12].

In this chapter, we outline the Mexican experience, including community engagement and social assessment, in implementing a Wolbachia-based strategy intended to suppress the natural population of Ae. aegypti in San Pedro Chimay, a Mayan indigenous location situated in Yucatan, Mexico.

2. Principles of community engagement

Projects based on IIT-SIT require models or frameworks for the community engagement process and activities. Every approach has its own strengths and limitations, but they offer guidance for the implementation of the plan of action. The center for disease control and prevention has developed a guideline that provides an interesting system that integrates steps for a successful engagement [17].

Before the intervention: (1) Establish clear purposes and goals; (2) address the main characteristics of the community (culture, economics, politics, norms, and values) and the experiences with other projects in the past or present.

For engagement to occur: (1) Establish a bond of trust with the community and their formal and informal leaders, as well as other local organizations; and (2) respect the self-determination of the community.

For engagement to succeed: (1) Build partnership with the community in order to create changes and improve topics related to health; (2) acknowledge the internal diversity of the community and the relations during the whole process of community engagement; (3) the engagement can be sustainable by the appropriation of the community; (4) the community must be involved from the beginning, be prepared, and develop decisions capacity in order to the sustainability of the engagement; and (5) the community collaboration demands wider commitment by the engaging of all sort of interested actors.

Therefore, the community engagement of the project, based on those principles for community engagement, was divided into four phases (Table 1), each one addressed in a transversal way the guidelines to express the social inclusion of the community targeted. Detailed information of each phase was already published elsewhere [12].

I. Preparation of the community	II. Prereleasing activities	III. Releasing activities	IV. Postreleasing activities
Rapid social assessment of the feasibility of the community	Social research on mosquito-borne diseases and social acceptance of the project.	Social license of the leaders and community through workshops.	Follow-up educational activities and social assessment of the perceived benefits.
Surveillance of social impact for the implementation of the intervention.

Table 1.

Community engagement and social evaluation.

3. The mosquitoes in the Mayan culture

The very presence of the mosquitoes in the Mayan culture had been represented with ambivalence, as an unpleasant pest, a hero, and an ally. Archeological evidence in both pre-Columbian pottery and Codex portrayed the mosquito sucking women’s breasts [18], while she tried to swat it (Figure 2). However, the narratives and interpretations are far from the current conception of the mosquito (transmitter of diseases). The plot is associated with the mythological personification of a disguised god (as a mosquito) that tries to marry the maiden represented, against the will of the father-in-law.

Figure 2.

Mosquito biting a maiden’s breast [18].

In the Mayan sacred book called Popol Vuh, there is a narrative about a mythic journey to the Xibalbá (Mayan underworld) led by the mythical twins Hunahpú and Ixbalanqué. In their trek, they needed to figure out the name of all the gods and gave the mosquito a mission in this plot, to push them to reveal their names, that says:

“Bite them one by one; first bite the one sitting on the foreground and end up biting them all, because that is the part that corresponds to you, sucking the blood of man on the road.” [19]

Although no associations were linked to mosquitoes as the transmitter of diseases in pre-Columbine documents, there are historical mentions of a plague called in the Mayan language “xekik” (vomiting blood) that was associated with yellow fever [20, 21], but once again no mentions of the mosquito as the carrier of any pathogens were proposed.

In the Mayan culture, there is a worldview classification of the arthropods associated with medicine, economics, food, and religion [22]. The mosquito does not seem to be included here, but only in contemporary studies [23, 24, 25, 26] we can identify the association with diseases, such as dengue.

Social research on cultural understanding of mosquito-borne diseases is as important as the study of the perceptions toward their vectors. Local taxonomies and ethnoecological approaches that frame the political, historical, and cultural context of this topic, shape the way people learn, think, represent, and take action for preventing practices [27, 28, 29, 30].

4. Uts k’oxol: a cross-cultural approach for IIT-SIT

In Yucatan, Mexico, 43.8% of the population are Mayan speakers and most of them live in Merida and the surrounding villages because of the urbanization, immigration, and economic changes [31, 32, 33, 34]. The releasing site of Wolbachia-infected mosquitoes, San Pedro Chimay, is part of those communities and the indigenous knowledge of the relationship between society and nature plays a key role in the community. Hence, a cross-cultural approach was considered to design strategies and materials for the engagement and social assessment [15, 16].

In the formative stage of the project (phases I and II, see Table 1), anthropological diagnosis and research were performed which aims to validate the feasibility of the community for the activities and the social acceptance of the whole process [15, 16]. To pursue the change of paradigm “from kill to release mosquitoes”, the necessity to transform scientific speech of the IIT-SIT methods into more appropriate local linguistic frames, meetings were organized to discuss the best way to achieve this goal. Most of the attendants, elders, and community leaders, acknowledged the value of using the Mayan language to communicate the main messages and goals of the project itself. During extensive discussion sessions about the challenges and benefits, they came out with the idea in the Mayan language of “Uts k’oxol” (translation: uts = good; k’oxol = mosquito) as a cultural-sensitive brand. The novelty of this achievement is that the team and the local leaders, created a new word, even for the indigenous worldview, to introduce IIT-SIT strategy in Yucatan, Mexico.

5. Social assessment of perceived benefits and disadvantages

The social assessment study was conducted in the sub-urban and Mayan indigenous community of San Pedro Chimay, which belongs to the municipality of Merida (capital city), the capital of the state of Yucatan located in the southern region of Mexico. This locality comprises 1246 inhabitants, 646 men and 615 women, and 305 houses [35]. However, the scientific team identified that only 150 dwellings were occupied by families able to participate in the project.

A semi-structured interview was applied to 70 participants heads of family of the community (December 2019 – February 2020). The design included both quantitative and qualitative questions that addressed several topics, such as profile of participants, reasons for participation in the activities, perceived characteristics of both wild and released mosquitoes, and the perception of the benefits and disadvantages of the project. In addition, an ethnographic approach was performed to gather information about the cultural contexts of the social assessment.

The information from the interviews was analyzed in two steps described as follows: quantitative data was processed using Microsoft Excel™ spreadsheets (2019), and qualitative data were explored in MaxQda software (2020). Both results were compared to create categories related to each aspect of the interview. In addition, ethnographic data were systematized within the emerged categories identified in the interviews.

5.1 Profile of participants

The semi-structure interview was applied to 70 heads of family in the community, 74.3% (52/70) were women and 25.7% (18/70) were men. 77.1% (54/70) were married, 11.4% (7/70) divorced, 11.4% (8/70) single, and 8.6% (6/70) were widow. About the education level, 57.1% (40/70) had elementary school level, 21.4% (15/70) had middle school, 8.6% (6/70) had high school level, 2.9% (2/70) had bachelor’s degree, and 10% (7/70) never went to school. All the participants (100%, 70/70) were both Spanish and Mayan speakers. Spanish was mostly used at workplaces, for traveling, and for business or education activities. In turn, Mayas were used more for domestic and private conversations among adults.

5.2 Engagement and participation in activities

As part of the engagement process, since the very beginning of the project, people were invited to several activities, such as workshops, community meetings, and educational demonstrations (Figures 3 and 4) [15, 16]. However, as expected, not all the families could participate in every phase of the intervention. A 42.9% (30/70) of the interviewed participants reported to be actively involved, while 57.1% (40/70) did not. Here, qualitative data help us to understand this divergence. For the people that embraced the actions and events, they said to recognize the importance of mosquito-borne diseases and they liked to participate in the project. The primary obstacles that the second set of members encountered were a lack of time, health problems, domestic issues, and the fact that they worked all week outside of the community.

Figure 3.

Demonstration activity “hand-cage”.

Figure 4.

Male mosquito releasing activities with school children.

This evidence framed a critical situation to achieve the engagement of a whole community, where families just cannot take part in it, regardless of the reasons. This is perhaps the main reason people interviewed asked for more house-to-house visits and the distribution of brochures because for them it is the best mechanism to be informed about the goals, processes, and benefits of the intervention. In words of a housewife and domestic worker woman interviewed, she said:

“To go to workshops is a luxury of time that I don’t have. My family must eat, my kids need to go to school, and this is not an easy thing for me and my family. Here in San Pedro [release-site], there are more women like me, this is real life.”

5.3 Perceived characteristics of wild mosquitoes

People were asked about the characteristics of the wild mosquitoes that they knew before the project started. 52.9% (37/70) reported that those mosquitoes are transmitters of diseases, 22.9% (16/70) said that mosquitoes do not transmit any disease, and 24.3% (17/70) were not sure about this aspect. A 45.7% (32/70) of participants reported that the female mosquito is responsible for this transmission of diseases, 4.3% (3/70) said the male mosquito, 5.7% (4/70) told both male and female, and 44.3% (31/70) were not sure.

In addition, people’s narratives and descriptions of experiences reflected a qualitative pattern emerged, such as “they are black with white stripes on their legs,” “it’s a big mosquito,” “it is called Ae. aegypti,” “they are black mosquitoes,” “there are female mosquitoes,” and “they bite.”

A 57.1% (40/70) reported that the female mosquitoes presented a blood-feeding behavior, 7.1% (5/70) identified the male mosquitoes with the same feeding pattern, 5.7% (4/70) believed that both male and female bite for human blood, and 30% (21/70) did not know about it. The information presented is a portrait of the general feature of the Ae. aegypti, the main mosquito in the community.

5.4 Perceived characteristics of released mosquitoes

Overall, 55.7% (39/70) reported that the mosquitoes released by the scientific team were females, 5.7% (4/70) told that they were male mosquitoes, 7.1% (5/70) both male and female mosquitoes, and 31.4% (22/70) did not know. To obtain a deep understanding of lay knowledge, people were asked to give their daily narratives of the presence and co-habitations of the released mosquitoes. Categories were developed to structure the verbatim provided by the participants, as shown in the following Table 2, top-down in order of most frequently mentioned.

Categories	Narratives
Feeding-behavior	“Male mosquitoes that do not bite”
Mating-behavior	“They are male mosquitoes that when mating with local females, their eggs will not hatch”
Wolbachia-references	“They are mosquitoes with Wolbachia”; “They have a chemical substance for the female mosquito to die”
Block-transmission	“They are mosquitoes that do not transmit Dengue, Chikungunya or Zika”
Reduce-mosquitoes	“They are mosquitoes that will help to reduce mosquitoes that transmit diseases”; “They are mosquitoes to hunt or kill female mosquitoes”; “The released mosquitoes will eat the bad mosquitoes”; “To catch other mosquitoes”
Name-Aedes aegypti	“They are Aedes aegypti mosquitoes”

Table 2.

Narrative descriptions of the released mosquitoes.

5.5 Perceived benefits and disadvantages

Overall, the majority of the interviewed perceived a positive benefit of the intervention, although there were people that did not acknowledge any advantage of this (Table 3).

Description	%/n
Reduction of mosquitoes	43% (30/70)
Help to prevent mosquito-borne diseases	26% (18/70)
Does not know	16% (11/70)
No benefits perceived	10% (7/70)
Learnings about mosquito-borne diseases	5% (4/70)
Total	100% (70/70)

Table 3.

Perceived benefits of the project.

In addition, the participants related their experiences about the advantages and benefits of the project.

“The truth is that it is a great benefit to reduce the risk of diseases in San Pedro. There are not too many mosquitoes that bite.” (Man interviewed, 22 years old)

“It is about preventing mosquito biting. Is the benefit that we learnt.” (Women interviewed, 60 years old)

“You must keep informed to avoid misunderstandings and gossip and the people will understand and acknowledge what you are doing.” (Women interviewed, 36 years old)

“We have to work with the people that believe those released mosquitoes are the bad ones because they are stubborn.” (Women interviewed, 67 years old)

On the other hand, 64.3% (45/70) of the participants reported no complaints about the released mosquitoes, while 35.7% (25/70) did. In-deep questions were asked to the last group about the reasons for the disadvantages and that must be addressed with a specific context. The two main reasons were identified here, mosquito’s nuisance at bedtime (35.5%, 25/70) and an increase of mosquitoes during the releasing days (37.2%, 26/70). In the community, families usually keep the doors and windows open during the day and rarely use bed nets or house-screening [15]. Thus, this facilitates the entrance of mosquitoes at any time given.

During the fieldwork, ethnographic data collected evidenced the concern of the elders of the community about the transmission of the Wolbachia to other organisms, such as bees and humans. In San Pedro Chimay, there is a strong presence of peasants that work in corn fields and beekeeping. In their experience, crop pests and diseases for bees are a huge problem. Therefore, they were worried about the unknown organism carried by released male mosquitoes.

5.6 Social acceptance of the project

At the beginning of the project (2017), a study was carried out addressing cultural barriers, strengths, and social acceptance of the intervention [15]. At the end of the project (2020), people were asked again if they would be interested in continuing to participate. 94.3% (66/70) of participants agreed, 4.3% (3/70) said no, and 1.4% (1/70) were not sure. The positive perception of the interviewed were supported by many experiences such as that the project was helping to improve the community’s health, other general benefits perceived (knowledge about domestic prevention against mosquitoes), and they were very interested in the main effect perceived, the reduction of the mosquitoes in their houses.

6. Conclusion

This research was conducted to evaluate the perceived benefits and disadvantages of an IVM control of the Ae. aegypti that included the release of male mosquitoes for the suppression of the mosquito population in Yucatan, Mexico. Previous studies reported a good social acceptance [15] and the educational approach regarding this innovative method [16]. As main conclusion, the population interviewed for this chapter, considered that the intervention is an important initiative, and as with every new strategy it comes with some challenges to be addressed.

6.1 Mosquitoes: Friend or foe?

For decades the purpose of the vector control programs was focused on killing the mosquitoes rather than increasing their number. The change of paradigm, from “kill to rear and release” demands a strong community engagement [36, 37, 38, 39, 40, 41, 42, 43]. Hence, the main challenge is not only the social acceptance of the early stages but the community support and social license until the closure of the projects based on these new biological vector control methods.

In Yucatan, Mexico, there are socio-anthropological studies about diseases, such as dengue, chikungunya, and Zika virus [23, 24, 25, 28, 29]. However, more research is required with an ethno-entomological approach, that is, focused on the local cultural understandings of the mosquitoes besides the learned knowledge from the government campaigns [27, 30]. Research conducted in Australia, based on innovative biological control methods, showed important perceived differences in the characteristics of wild mosquitoes [38]. Although education activities about the taxonomic differences between male and female mosquitoes were explained to participants at the release site, still residents mentioned the similar appearance among different species of mosquitoes. In our study, ethnographic data evidenced that the participants identified at least one or two characteristics of the Ae. aegypti; however, residents that could not be involved in the project (workshops and demonstrative release activities), hardly reported the basic aspects of the mosquitoes [16]. This is a very important issue because the strategic discourse of “reduce Ae. aegypti mosquitoes” can be confused with “reduce all the species of mosquitoes” in the community, and, as a result, misunderstandings on the efficacy of the method might arise.

6.2 Community engagement for IIT-SIT: Challenges and experiences

According to the CDC’s principles for community engagement, the transversal path is key to all the phases, processes, and actions for the implementation of the project. All three steps of this model had to be reinforced along the development of the activities.

The goals need to be presented in different formats and for several audiences (adults, children, and elders) and languages (Mayan-Spanish). Also, unexpected political scenarios took place during the beginning, such as political elections at national and local level, which required changes in the leader-engagement strategies because the whole municipal committee was new, and all the political landscape changed. Therefore, the bound of trust initially constructed demanded the inclusion of other informal actors in the arena, and with this unrepresented groups of the community emerged.

To respect the self-determination of the community, there was a flexible partnership collaboration to build that could include more social groups, even with political and cultural differences, to become part of the decision-making process. The very sustainability of the project was once again challenged by another unexpected situation, that is, the COVID-19 pandemic. We conducted an additional social evaluation addressing if the leaders will be agreeing that the project could be continued, with minimal activities (entomological surveillance and mosquito-releasing activities following the proper preventive measures), but the result was that they preferred to put it in stand by the project until the pandemic event ends.

Finally, it is important to highlight that social license was a key factor for the success of the intervention and should be part of innovative paradigms for mosquito-vector control strategies involving community engagement. In this chapter, we outlined the Mexican experience of community engagement and social assessment in implementing a Wolbachia-based strategy intended to suppress the natural population of Ae. aegypti.

Acknowledgments

Abdiel Martin-Park is supported by the Catedras-CONACYT program. Research funding was provided by Fondo Mixto Consejo Nacional de Ciencia y Tecnología (CONACYT) (México)–Gobierno del Estado de Yucatán (project YUC-2017-2103-01-556) and U.S. Agency for International Development (USAID) (project AID-OAA-F-16-00082). In addition, special thanks to the people of San Pedro Chimay and the personnel of the Ministry of Health for supporting during the project and field activities.

Conflict of interest

The authors declare no conflict of interest.