Introduction

Since the beginning of the 21^st century, dengue fever has been a significant vector-borne arboviral disease, occurring mainly in tropical and sub-tropical countries where more than 3.9 billion people are at risk of infection in 128 countries [1–4]. With an estimated 400 million annual dengue incidence worldwide, the disease is currently endemic in more than 125 countries in Africa, the Americas, South East Asia and other regions in the world [2]. Sixty percent of dengue cases occur in the Americas, predominantly Latin America, where the disease has re-emerged owing to re-infestation by the dengue vector. Since its re-emergence in Latin America, dengue has spread dramatically throughout the region [5]. The number of reported dengue cases rose from 1,033,417 in the 1980s to 2,725,405 in the 1990s, and 4,759,007 between 2000 and 2007 [2, 5]. Between 2001 and 2009, six countries accounted for more than 75 percent of all cases in the region: Venezuela, Brazil, Costa Rica, Colombia, Honduras and Mexico [6, 7]. Various political, environmental and social factors influenced the re-emergence of the disease in Latin America. Dengue is largely an urban disease [7]. Overcrowding, uncovered water sources and climate change are optimal conditions for geographic spread of the mosquito vector for dengue, which lives in domestic settings and can breed in very little water and survive drought conditions [1]. The impact of urbanization is particularly significant in low and middle-income countries [8–10].

Among the South American countries of Argentina, Brazil, Chile, Paraguay and Uruguay, Brazil has the highest incidence rate of dengue with 294 cases per 100,000 inhabitants in 2014 [11]. Brazil is considered a tropical country in its entirety because of its hot and humid climate, which provides a favorable environment for proliferation of the dengue vector. Incidence of dengue in Brazil has frequently been high, and the number of cases in the country has sometimes represented as much as 60% of all reported dengue cases worldwide [11]. After the disruption of its vector control program, Brazil experienced a series of dengue outbreaks [5, 11] characterized by increasing geographic spread and severity as estimated by the number of hospitalizations and deaths [11]. In the first eight months of 2015, Brazil experienced an increase in dengue of 140 percent over the same period during the previous year (1,416,179 cases from January to August 2015 versus 589,107 cases in 2014). During that same period, the number of severe cases increased dramatically (1,284 severe cases in 2015 versus 664 severe cases in 2014) as did deaths (693 deaths in 2015 versus 407 deaths in 2014) [11].

Dengue imposes significant economic and societal burdens on countries where the disease is endemic and, as such, estimating the associated disease impact can help inform policymakers and assist them in setting priorities for disease control and management strategies [12, 13]. The effects of dengue on health and preventive care, its economic burden and social impact on populations have not been clearly studied. Understanding dengue burden from societal and socio-economic perspectives is crucial for allocation of limited scarce public health resources among competing health threats, as well as ensuring cost-effectiveness of integrated dengue prevention and control methods.

One such method promoted by the World Health Organization to overcome challenges associated with conventional single-intervention approaches is Integrated Vector Management (IVM). Defined as a “rational decision-making process for the optimal use of resources for vector control,” IVM considers five key elements in the implementation of IVM to prevent vector-borne diseases such as dengue: advocacy, social mobilization and regulatory control; collaboration within the health sector and with other sectors; integration of non-chemical and chemical vector control methods; evidence-based decision-making; and development of adequate human resources, training and career structures [14]. The growing burden of dengue and the challenges of preventing dengue outbreaks (including increase in prevention costs such as on vector control) have increased the urgency of the public health sector to identify alternative management strategies [15–19]. Monitoring of public impact, perceptions and behaviors is needed in order to guide the development of adequate and effective strategies to controlling and preventing dengue outbreaks. Establishing key performance indicators is important in measuring the effectiveness of existing and current surveillance and vector programs. In addition, identifying and understanding societal, cultural and environmental factors related to dengue outbreaks may provide insight for the development of targeted dengue prevention and control interventions, including community involvement and engagement in vector control activities given that community-based interventions have been found to impact vector indices [20]. Furthermore, understanding dengue vector-virus-disease behaviour and human-animal-environment interactions and interdependencies, known as “One Health,” is critical to IVM [21]. This can provide early and timely added value for consolidated and harmonized mitigation and adaptation tactics and advocacy in local settings [22].

Given the dearth of literature, qualitative studies are needed to gain in-depth understanding of stakeholder and community reactions to a dengue outbreak and its related impact. The growing burden of dengue in Brazil presents an interesting model for qualitative research around the challenges and issues that need to be addressed to strengthen dengue prevention and control interventions in Brazil and throughout Latin America.

The objectives of this study were to understand the impact of dengue outbreak on different stakeholders in Brazil, to explore stakeholder perceptions of approaches used by governmental authorities to control and prevent dengue outbreaks and to define the challenges and implications of preventing future outbreaks.

Methods

Results

Participants

A total of 40 stakeholders were included in the study, with 18 stakeholders in São Paulo State (Marília and Sorocaba municipalities) and 22 in the Rio de Janeiro State (Búzios and Rio de Janeiro municipalities). The different stakeholders included in the study were physicians (Phy), nurses (Nu), hospital administrators (HA), community members (CM), community leaders (CL), school administrators (SA), municipal policy makers (MPM), vector control managers (VCM) and business leaders (BL) (Table 1).

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Table 1. Categories of stakeholders included in the study, April—August 2015, Brazil.

https://doi.org/10.1371/journal.pntd.0005366.t001

The study included three physicians and three nurses from a public facility and one physician and one nurse from a private facility. Two hospital administrators were from a private facility and one from a public facility. One nurse and one physician from separate private hospitals also had previous experience working in a public emergency care center during a dengue outbreak.

Discussion

The study shows that a dengue outbreak undermines medical, social, societal, economic and political stability through a rapid patient influx into the healthcare system, the financial burden on governments and households, and the effect of community dissatisfaction and disengagement on outbreak control measures. This multi-sectorial impact, although limited, results in social and political disruption. In addition to providing a description of the challenges that need to be surmounted during dengue outbreaks, this study suggests important considerations that should be accounted for in the design and implementation of future dengue prevention and control interventions.

For the majority of stakeholders interviewed in this study, dengue control and prevention efforts implemented by the authorities were seen as insufficient. As citizens witnessed the rapid growth of dengue cases in their communities, fear and anxiety for contracting the disease impacted social structures. Stakeholders expressed frustration over the lack of concerted and timely government efforts to prevent and control outbreaks in the community, and many did not perceive the impact of such interventions. Stakeholders also felt that prevention efforts did not appear to be sufficiently coordinated. Insufficient governmental response or late responses to outbreak management appeared to generate a lack of confidence from the community. As a result, communities became increasingly disengaged and uninterested in vector control efforts in their household or neighbourhoods. Our findings underline the importance of permanent and strong social mobilization efforts and concerted community interventions in dengue prevention and control and the difficulty in maintaining mobilization efforts in the community over time [19].

In regards to healthcare system, the significant and rapid influx of patients placed a major burden on public and private health facilities as they struggled to find the space and the staff to handle demand and the means to minimize increasingly long patient waiting times. Planning around potential outbreak scenarios prior to an outbreak and improving dengue case management in health facilities during outbreak periods is a priority in ensuring improved clinical outcomes and quality of care. This is particularly critical in cities with limited infrastructure and human resources.

The study provides a significant description of the challenges that need to be surmounted during future dengue outbreaks and suggests important multifocal approaches that should be developed to meet these challenges. Indeed, the results of this qualitative study mirror studies done in other regions in the world, such as Southeast Asia, Ecuador and Mexico, with regard to economic burden and effects on community and municipal functions [13, 25, 26]. Poor populations are greatly impacted and approaches to education need to be improved. A better community understanding of approaches to dengue control is important to their successful implementation [8, 14, 27, 28]. However, development of these educational programs requires knowledge of the culture, organization and functioning of community members and local authorities [14, 28, 29]. Such knowledge can be obtained by exploring the community’s level of understanding of dengue outbreaks obtained from information communicated by governmental authorities, media (newspapers, radio, TV) and social networks.

To better manage and increase confidence of community members in vector control actions, protocols specifically designed for the local environment that can be rapidly implemented at the beginning of an outbreak need to be further developed [30]. Planning should include improved approaches to educating community members and leaders about dengue, increasing the availability of dengue resources before outbreaks and maintaining necessary resources and services between outbreaks. During outbreaks, local sensitization campaigns must focus on community mobilization activities to eradicate mosquito breeding. Knowledge or awareness has been reported as being important for the success of dengue prevention and control efforts, and inadequate knowledge about dengue was found to be a major impediment to the successful implementation of approaches used to eliminate dengue. Importantly, studies indicate that dengue knowledge alone did not single-handedly translate to adoption of preventive measures. Instead, policy makers and planners must also focus sensitization campaigns on reducing barriers to behaviour change related to control of dengue fever among the population [16, 31], and encouraging communities to adopt preventive measures [16]. Such actions should increase community confidence in government responses to dengue outbreaks while decreasing fear and misconceptions. Increasing the confidence of community members would also be expected to decrease the chances of political breakdown, a concern of community and government leaders during an outbreak.

Dengue prevention and control should include individuals, families and the wider community and encourage community participation to improve its chances for success. In a routine dengue prevention and control program, a community based environmental strategy showed a significant reduction in levels of Aedes infestation by 50–75% compared with a routine program without community involvement [19]. Comprehensive and enhanced dengue intervention strategies based on community engagement could have a significant and effective impact on dengue outbreak control, yet are highly dependent on the community’s perception of the severity of the disease. Intervention strategies should be built into existing health care systems and closely coordinated with the national dengue control program [29, 30].

The cost of dengue control at the household level also needs to be addressed in relevant protocols and community mobilization activities, particularly with regard to the allocation of resources during an outbreak and with planning for poorer populations. In this study, lower income populations also reported more challenges in covering the cost of treatment, or difficulty paying indirect costs, such as transportation charges for hospital or health facility visits [13].

While this study was not intended to quantify the economic impact of the disease, the financial data gathered highlights the substantial investment needed to cover the cost of on-going prevention and control efforts. At least R$ 4.2 billion (US$ 1.28 billion) was spent on dengue control and prevention efforts between 2010 and 2014 in Brazil [23, 24]. At the federal, state and municipal levels alike, the financial burden of dengue is significant and multi-sectoral. State and federal contributions may not always be sufficient to meet municipal prevention and control needs. For example, Sorocaba’s spending in 2015 for dengue control and prevention was an estimated R$ 11 million (US$ 3.5 million) for the full year, nearly twice the total amount distributed by the state to all 645 municipalities in São Paulo [32, 33]. The results also emphasize the critical challenge around financial accountability for dengue control and prevention among levels of government and the limited impact of costly year-round campaigns. LR Carasco et al. demonstrated that the average economic impact of dengue illness in Singapore from 2000 to 2009 ranged between US$0.85 billion and US$1.15 billion, of which control costs constitute 42%–59% [34]. A 2013 study conducted in 12 countries in Southeast Asia showed that, there was an annual average of 2.9 million (m) dengue episodes and 5,906 deaths from 2001–2010. The annual economic burden (with 95% certainty levels) was US$950 million (US$ 610million—US$ 1,384million) or about US$1.65 (US$ 1.06 —US$ 2.41) per capita. A study conducted in four Brazilian regions estimated that the cost for dengue prevention and control for the epidemic season in 2012–2013 was substantial [35]. The annual national economic burden was US$ 164 million from the public payer perspective, but may be as high as US$ 447 million (adjusted for underreporting). From the societal perspective, the economic burden was US$ 468 million, but may be as high as US$ 1,212 million [35].

In addition to the medical, economic, social and political impact of dengue, this study also found that another key factor contributing to the need to prioritize dengue is that it is a highly visible disease. This visibility is due to the fact that dengue often occurs in epidemics, which attracts media attention, stokes public fear and puts a strain on municipal budgets. This is in contrast to non-epidemic diseases, such as diarrheal disease and pneumonia, which attract less public or media attention [36]. For this reason, community engagement and satisfaction is particularly important in the dengue context. Furthermore, given the visibility of the dengue, the role of the media during dengue outbreaks should be better understood. Appropriate and effective management approaches, ready to deploy before a dengue outbreak occurs, would decrease the burden on health care facilities, increase the confidence of community members in government responses to outbreaks and would keep municipalities operating with increased efficiency. Increased confidence of community members would also be expected to improve community involvement and compliance with official approaches to dengue control. Improving community involvement and compliance during dengue outbreaks should decrease the intensity and duration of the outbreak and decrease the chances of subsequent outbreaks [37].

Recently, a long-term follow-up and integrated efficacy analysis of 35,000 children between the ages of 2 and 16 years in Asian Pacific and Latin American countries showed a reduction in dengue disease in the efficacy surveillance phase among children and adolescents who received a recombinant live attenuated tetravalent dengue vaccine. The vaccine was also associated with a lower risk of hospitalization and severe dengue overall up to 2 years after completion of the three-dose vaccination schedule among children 9 to 16 years of age [38]. Disease impact modelling has further indicated that if 20% of the populations in the 10 countries that participated in these efficacy studies were vaccinated, this could potentially reduce dengue burden by 50% in these countries [39]. Improved approaches to dengue management that include the considerations discussed in this study will continue to play a key role in a comprehensive prevention and control strategy. Future research should include gaining an understanding of how a vaccine would help the local community, including analysis of the cost- effectiveness of a vaccine program and the impact of vaccination as part of an integrated prevention strategy for dengue in endemic countries [35, 40]. Initiation of a public dengue immunization program could serve as a long-term and visible commitment by leaders to protecting populations against the economic and human impact of this disease, and hence may contribute to regaining public trust in governments where public confidence has been affected by a dengue outbreak.

This study presents limitations. First, the results should be considered in the context of the study sample size and the nine categories of stakeholders included, with an unequal distribution of stakeholders per category. The unequal distribution is partly associated with difficulties faced in identifying voluntary participants in select stakeholder categories directly involved in prevention and control measures given the sensitive nature of the topic at the time of the study. In certain stakeholder categories there may exist some limitations to data transferability, yet in most categories, data saturation was achieved. Secondly, since the study is qualitative and explorative, caution must be used with interpretation of the results. Further investigations will require other methodological approaches such as quantitative methods to confirm our findings. In addition, while the value of focus group discussions in presenting varying opinions and perspectives is recognized, the sample size of the study did not permit for such an approach. Thirdly, the sample of informants may not have included all major stakeholders in each municipality or have been representative of all stakeholders. As with all qualitative studies with open-ended responses, there is also the possibility of misunderstanding or biased interpretation of participant responses. Nevertheless, the strength of this qualitative study lies in the sample comprised of a large panel of stakeholders from a diverse socio-demographic background, which closely resemble the population usually involved in dengue control. The structure of the interviews, which allowed for probing and clarification of responses, and analysis were designed to minimize misinterpretation.

In conclusion, the study provides useful insights from different stakeholder populations that could guide local authorities and government officials in planning, designing and implementing integrated public health programs and activities aimed at preventing and controlling dengue in Brazil. The consequences of a dengue outbreak reach far beyond the people infected, undermining medical, social, economic and political stability. Ultimately, an effective means of preventing dengue outbreaks that combines vector control and vaccination would reduce the social and political disruption and economic impact of the disease. The recent explosive outbreak of the Zika virus in South America reinforces the urgent need for more integrated research and public health strategies to control arboviral diseases [41, 42]. Similar to the qualitative study reported in this paper, research that is designed to understand how a community and its local government responds to dengue outbreaks and two other arboviruses (chikungunya, Zika) circulating in Brazil, is a necessary component for designing and implementing plans to decrease the incidence of dengue outbreaks in Brazil. Such research will inform public policy by providing evidence-based recommendations to decrease the burdens of dengue outbreaks on both communities and governments

Supporting information

Acknowledgments

The authors would like to thank all the stakeholders interviewed for their time and their contributions.

Special thanks to M Charlie Spieholz for manuscript editing.