Prevention and control of mosquito-borne arboviral diseases: lessons learned from a school-based intervention in Brazil (Zikamob)

Since the 1980s, when dengue was reintroduced in Brazil, outbreaks and epidemics caused by different arbovirus strains transmitted by vector mosquitoes such as Aedes aegypti (A.e) have been an annual occurrence [1]. Since 2010, it has been estimated that there have been over a million cases of dengue per year, leading to hundreds of deaths [2]. Since 2015, with the introduction of the Zika and Chikungunya viruses in the country, cases have been reported of children with congenital Zika syndrome or chronic sequelae [2]. The similarity of symptoms, cross-reactivity, co-circulation and overlap of infections by different arbovirus species and strains make the differential diagnosis of these diseases difficult [1]. The main strategy for reducing the prevalence of these diseases has been vector control with larvicide application in water tanks and spatial nebulization with insecticides widely used in the control of adult specimens [3], which has contributed to the selection of resistant insect strains [4]. The development of vaccines and alternative control methods using transgenic bacteria and mosquitoes has also been reported in the literature [5, 6].

The engagement of the population in preventive actions is one of the main objectives of vector control policies, given that most of the breeding sites are located in households and on vacant land and abandoned houses [7, 8]. This engagement has been stimulated and supported by mass media advertising, the use of breeding reporting applications (eg Zikazero) [9] and environmental education by home-visiting performed by health workers [7, 10]. Unfortunately, in urban centres in Brazil, these visits often do not occur because residents are not in their homes or they do not allow health workers to enter for inspection and guidance on vector control for fear of violence [11]. In this context, the implementation of interventions in schools using digital platforms for mobile devices can be a powerful tool for the promotion of engagement by the population in preventive actions for arboviruses, and this can be directed by entomological surveillance services.

The World Health Organization has recommended grounding educational interventions in behaviour change theories [12, 13], considering the growth of evidence for their effectiveness at individual, community and population levels [14, 15]. The Health Belief Model (HBM), for example, suggests that decision-making depends on the perception of susceptibility, disease severity, benefits and barriers associated with behaviour [12, 16]. Social Cognitive Theory (SCT) describes three main factors that affect a person's likelihood of changing health behaviour: self-efficacy, goals, and outcome expectations [12, 17]. Even small changes in human behaviours can have substantial effects on population health outcomes [13].

Building on these behaviour change theories, the aim of this study was to evaluate the behavioural change of high school students and teachers who participated in a virtual educational intervention. This is the third stage of the project, “Impact of mobile learning on prevention and management of complications caused by arbovirus (Zika, Dengue, Chikungunya) – ZikaMob,” funded by the British Council and the Government of Paraíba State, in Northeastern Brazil.

Of the 883 survey participants, 690 were students ranging in age from 14 to 41 years, with an average of 17.1 ± 2.5 years; and 193 were teachers from 22 to 64 years old, averaging 38.5 ± 9.2 years. In all, 510 (58%) participants were female: 393 students and 117 teachers (Table 1). Most participants (84%) owned a single-storey house with access to running water (97%), and only 13% reported lack of water for more than two days a week. In all, 34% reported using buckets to store water, 75% had water tanks and 21% had cisterns. Access to municipal waste collection services is virtually universal (96%). Of all households, 71% have a backyard where 51% of respondents grow plants or vegetable gardens. Around 55% of participants reported having abandoned houses or vacant lots nearby and 35% reported streams or sewers nearby their houses. On 64% of the land, there was trash that could serve as a mosquito breeding ground. In all, 37% of participants had unprotected roofs (i.e., no lining), potentially allowing mosquitoes to enter through the cracks in the tiles (Table 2).

The frequencies and results of Pearson's chi-square test on household and environmental risk variables for Study A (paired sample) were shown in Table 2, comparatively before and after intervention, respectively. No significant differences were found in the paired sample, indicating excellent reliability because the same participants answered identical questions before and after the intervention (Table 2). The Cronbach's alpha result for all categorical variables was 0.966, indicating excellent internal validity of the questionnaire used.

Regarding the comparison between students and teachers, a quite different pattern was found between the two groups in seven of the 14 variables. Teachers have greater financial stability and live more commonly in a well-built building and therefore have a lower risk of mosquito breeding in their homes (Table 2). In the study B (unpaired sample), more male students living in well-built buildings responded to Q2, giving rise to different risk conditions such as access to or lack of water (Supplementary Table 1).

In all, 85% of respondents reported helping with household chores; 75% assisting in the care of plants and gardens; 62% have observed mosquitoes in their homes, and 98% believe that it is important to make efforts to clean up waste land and homes to reduce the prevalence of mosquito-borne arboviruses (Table 2). Teachers do more housework and care more for plants and gardens than students do (Table 2). Results for the unpaired sample show differences in all facilitating behaviours in the student group, although the two data collection points may have different results because more men responded to Q2 (Supplementary Table 1) than had to Q1.

Of all participants, 36% said they had had dengue, zika or chikungunya. In both samples, there was a significant reduction in the self-reported prevalence of these diseases for family members after the intervention (Table 2). In all, 11% of participants mistakenly believe that dengue infection can occur only once in a lifetime and 8% stated that there is a vaccine available for this disease. Almost all participants (97%) recognized that dengue can lead to death and 84% were afraid of acquiring one of these diseases; however most (67%) believed that their risk of infection is low because they adopt preventive measures (97%) (Table 2).

In the paired sample, there was no significant difference in these perceptions before and after the intervention, except for preventive measures. One noteworthy feature was that teachers showed greater fear of acquiring these diseases (p<0.001), with significantly different perceptions of susceptibility and severity than students (p=0.003) (Table 2). In the unpaired sample, there were clear differences in students' knowledge with the intervention (i.e., there was a bigger pre-post difference to that shown by teachers) and there were varying degrees of difference in relation to all constructs when comparing teachers and students, reproducing the findings of the paired sample (Supplementary Table 1).

Regarding self-efficacy, over 90% of participants believed they were able to change their behaviour, and 84% felt able to change the behaviours of their families, friends, and neighbours (Table 2). Teachers believed more than students in their ability to convince others to change their behaviour (p=0.037). In the paired sample, contrastingly, after the intervention, participants reported a lower conviction in their ability to change (p=0.039), although they came to believe more that they could alter the practices of relatives and neighbours (p=0.019) (Table 2). In the unpaired sample, there was a significant difference between students and teachers for almost all responses except the belief in changing neighbours and family members (Supplementary Table 1).

This study showed that educational interventions using a virtual platform can promote behavioural change regarding arbovirus prevention, corroborating the findings of preliminary studies conducted with smaller samples [18, 19]. The use of the ZikaMob platform adapted for mobile devices facilitated effective teaching about arboviruses and their prevention, better organization against their spread, and greater performance of synchronous preventive actions involving students from different schools and neighbourhoods of the second most populous city of Paraíba, in northeastern Brazil. This is an innovative strategy that has the potential to be replicated in any location that has an internet network and can involve an unlimited number of participants as long as they have a mobile device. This study corroborates findings from the literature that describe interventions based on behaviour change theories [23] and use of digital technologies [24].

In Brazil, dengue prevention guidelines and policies have set social mobilization goals and directed calls for action at schools; however, they have not defined strategies for carrying them out. In this paper, for the first time in Brazil, we described the development of a platform that allows the inclusion of all students and teachers in a city in order to perform synchronized prevention actions which are disseminated through social networks, increasing the number of people affected by the actions. A systematic literature review has shown that complex population-oriented interventions are more effective in reducing vector mosquitoes than specific actions [25]. This study has also shown that multifaceted interventions involving the community and professionals from the fields of health, education, and the wider social infrastructure, including the mass media, are more likely to be effective for vector control.

Arbovirus vector mosquitoes proliferate during the rainy season [26, 27]; for this reason, preventive actions must be planned and implemented at certain times of the year in order to maximize their effects. Using the strategy described in this paper may facilitate the synchronization of these actions and allow for the establishment of a shared calendar between schools and health services, enhancing results and reducing costs related to human and material resources. The results of this work showed a clear change in population behaviour with the use of school interventions. Therefore, the revision of public policies related to vector control is recommended, in order to incorporate the model and strategies described herein.

In this project, the researchers publicized the project in all high schools in the city of Campina Grande; however, engagement was dependent on the individual and voluntary decision of teachers and school principals. To reward the teachers’ efforts and motivate them to participate in the preventive actions, an 80-hour continuing education course certificate was given to the participants that could be used as part of salary bonus requirements. Of the 490 teachers who registered, only 193 performed the proposed activities on the virtual platform, but there is a clear correlation: in schools where teachers engaged, more students also participated in the actions.

The mobilization and engagement of teachers, students, and the community in interventions to prevent arboviruses needs to be understood as a collective project and as public policy, with technical guidelines, timing and integrated management. Teacher dropout occurred because prevention actions were not part of the school's calendar of activities and were not considered a priority by the managers. These preventive actions were not foreseen in the action plans of schools or health services.

One of the barriers to the integration of preventive actions with arboviruses in Brazil is the lack of agreement between federative entities. Surveillance and environmental education services are the responsibility of municipalities, and the management of high schools is the responsibility of the state. Due to political differences, it is often difficult to develop joint action between municipal and state managers. In addition, as has occurred in other Latin American countries, there is a growth in urban violence that has hampered entomological surveillance actions [28]. In Campina Grande, health workers reported that they were unable to enter up to 70% of households for inspection because residents were working or did not allow them to enter for fear of being robbed [11]. The authors contend that, in urban regions, the traditional model of home surveillance performed by health workers in the context of urban violence should be investigated further and include an assessment of cost-effectiveness [11].

There is evidence in the literature of randomized trials showing the effectiveness of using window screens with or without insecticides [29], mosquito nets or curtains [30] to reduce the prevalence of dengue. In Brazil, the guidelines for vector control did not prioritize the use of screens on windows and doors, either with or without insecticides, as a mechanical barrier method to avoid direct contact with mosquitoes. Instead, vector control actions have been based on the use of larvicides and insecticides [31, 32], which has led to an increase in resistant mosquito populations [33]. In this paper, we found that the population was unaware of these preventive measures because they are not publicized in traditional government campaigns; and that there was a significant difference in the use of window screens due to the intervention.

Our outcomes showed that intervention improved recycling. The separation of solid waste with a donation to waste pickers is one of the behaviours that contribute to reducing social inequalities and improving the environment and the health of populations [34]. Plastics dispensed in inappropriate places such as gardens and open land serve as breeding grounds for mosquitoes [34]. In Brazil, the garbage is placed in plastic bags at the gates of households without separation of recyclables, as most cities do not offer selective collection service. Waste pickers, usually illiterate people in socially vulnerable situations, open their bags on the streets and take advantage of recyclables, often leaving the garbage scattered. When the population separates the recyclables, this increases the income of the pickers. In this paper, a strategy to articulate the actions of entomological control to those of recycling was evidenced. By sorting and donating recyclables to waste pickers, people see a reward or benefit in changing their behaviours. To date, this was the first intervention study to establish the link between home inspection and recycling actions.

Most of the participants in this study reported fear of acquiring arboviruses, but the perceived risk is low, corroborating findings from another study in French Guiana [4, 35]. Students showed lower risk perception than their teachers or health workers [19]. Younger individuals tend to have lower risk perception and lower concern about acquiring arboviruses [4, 35, 36]; as do women of reproductive age [37]. Risk is higher among pregnant women than non-pregnant women [38, 39] and there is also a higher rate of disease acquisition in this group [40]. Living in an area with a higher prevalence of the disease does not change the perception of risk and susceptibility [35, 40].

In Pakistan, logistic regression analysis showed that perceived risk and self-efficacy are predictors of dengue prevention practices [40]. Regarding self-efficacy, we found that the participants in this study believe they can change their behaviours, and those of their family members, colleagues and neighbours. With the intervention, participants began to reflect more on their ability to convince others to take collective preventive actions and the use of social networks to accomplish this.

Most studies on arboviruses in the literature describe perceptions and knowledge about arboviruses prevention [41, 42], with few reports of school-based interventions [43‐45]. Most of these studies, however, are not randomized case-control trials based on behaviour change theories that can offer evidence of intervention impact and effectiveness [39]. In Puerto Rico, for example, an intervention by the Department of Health in partnership with the Centre for Diseases Control and Prevention (CDC) from the United States was performed, which showed a significant impact on knowledge and preventive behaviour for dengue, and reduced rates of mosquito infestation [39, 46].

The limitations of this study concern firstly the fact that the questionnaire is self-reported and secondly the design of the study itself. However, the paired analysis showed that our data were reliable. To verify the impact of interventions, the ideal design would be a case-control study; however, in this work, teachers and students receive a reward (prize) for participating in the research; therefore, there was no way to create a “control group”. In addition, there is the possibility of using the Aedes aegypti Rapid Infestation Index (LIRAa) [20] that measures the level of vector mosquito infestation in urban strata (territorial units with 10,000 inhabitants) to assess the impact of educational intervention. These measures are performed by health workers three times a year and could be used to assess the impact of educational activities. However, to carry out this type of study it would be necessary for all high school students from Campina Grande to participate in the intervention, georeferencing these students and reducing the size of the LIRAa territorial unit and / or the joint definition of research involving the services of Environmental Surveillance and the Secretariat of Education [20]. Moreover, health workers should be integrated into educational activities. During the intervention research, their activities were mostly paralysed due to a strike.

The findings of this work show that school-based interventions can promote change in attitudes and behaviours in the population, which could lead to a reduction in infestation and a lower risk of illness and death from arbovirus.