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The impact of climate suitability, urbanisation, and connectivity on the expansion of dengue in 21st century Brazil

['Sophie A. Lee', 'Centre For Mathematical Modelling Of Infectious Diseases', 'London School Of Hygiene', 'Tropical Medicine', 'London', 'United Kingdom', 'Centre On Climate Change', 'Planetary Health', 'Theodoros Economou', 'Climate']

Date: 2022-01 

Abstract Dengue is hyperendemic in Brazil, with outbreaks affecting all regions. Previous studies identified geographical barriers to dengue transmission in Brazil, beyond which certain areas, such as South Brazil and the Amazon rainforest, were relatively protected from outbreaks. Recent data shows these barriers are being eroded. In this study, we explore the drivers of this expansion and identify the current limits to the dengue transmission zone. We used a spatio-temporal additive model to explore the associations between dengue outbreaks and temperature suitability, urbanisation, and connectivity to the Brazilian urban network. The model was applied to a binary outbreak indicator, assuming the official threshold value of 300 cases per 100,000 residents, for Brazil’s municipalities between 2001 and 2020. We found a nonlinear relationship between higher levels of connectivity to the Brazilian urban network and the odds of an outbreak, with lower odds in metropoles compared to regional capitals. The number of months per year with suitable temperature conditions for Aedes mosquitoes was positively associated with the dengue outbreak occurrence. Temperature suitability explained most interannual and spatial variation in South Brazil, confirming this geographical barrier is influenced by lower seasonal temperatures. Municipalities that had experienced an outbreak previously had double the odds of subsequent outbreaks. We identified geographical barriers to dengue transmission in South Brazil, western Amazon, and along the northern coast of Brazil. Although a southern barrier still exists, it has shifted south, and the Amazon no longer has a clear boundary. Few areas of Brazil remain protected from dengue outbreaks. Communities living on the edge of previous barriers are particularly susceptible to future outbreaks as they lack immunity. Control strategies should target regions at risk of future outbreaks as well as those currently within the dengue transmission zone.

Author summary Dengue is a mosquito-borne disease that has expanded rapidly around the world due to increased urbanisation, global mobility and climate change. In Brazil, geographical barriers to dengue transmission exist, beyond which certain areas including South Brazil and the Amazon rainforest are relatively protected from outbreaks. However, we found that the previous barrier in South Brazil has shifted further south as a result of increased temperature suitability. The previously identified barrier protecting the western Amazon no longer exists. This is particularly concerning as we found dengue outbreaks tend to become established in areas after introduction. Highly influential cities with many transport links had increased odds of an outbreak. However, the most influential cities had lower odds of an outbreak than cities connected regionally. This study highlights the importance of monitoring the expansion of dengue outbreaks and designing disease prevention strategies for areas at risk of future outbreaks as well as areas in the established dengue transmission zone.

Citation: Lee SA, Economou T, de Castro Catão R, Barcellos C, Lowe R (2021) The impact of climate suitability, urbanisation, and connectivity on the expansion of dengue in 21st century Brazil. PLoS Negl Trop Dis 15(12): e0009773. https://doi.org/10.1371/journal.pntd.0009773 Editor: Hannah E. Clapham, National University Singapore Saw Swee Hock School of Public Health, SINGAPORE Received: August 27, 2021; Accepted: November 24, 2021; Published: December 9, 2021 Copyright: © 2021 Lee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All data used in this study is open access and available freely on the internet, see the methods section for more details. Data and code used to produce this analysis is available from a Github repository cited in the manuscript (https://github.com/sophie-a-lee/Dengue_expansion). Funding: S.A.L. was supported by a Royal Society Research Grant for Research Fellows. https://royalsociety.org/. R.L. was supported by a Royal Society Dorothy Hodgkin Fellowship https://royalsociety.org/. T.E. was funded by the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 856612 https://ec.europa.eu/info/research-and-innovation/funding/funding-opportunities/funding-programmes-and-open-calls/horizon-europe_en and the Cyprus Government. C.B. was funded by the National Council for Scientific and Technological Development under grant No. 303985/2019-4 (http://www.cnpq.br/) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction Dengue is considered one of the top 10 threats to global health [1], with around half the world’s population living in areas at risk of infection [2]. Incidence rates have doubled each decade in the past 30 years as a result of increased urbanisation, global mobility and climate change [2–4]. All 4 dengue serotypes are endemic to Brazil, which experiences frequent outbreaks across the country [5]. Previous studies identified geographical barriers to dengue transmission beyond which regions were relatively protected. This included South Brazil, where seasonal temperatures are too cold for vectors to efficiently transmit the virus, areas of high altitude in Southeast Brazil and remote regions of the western Amazon [6]. However, these barriers are being eroded and the dengue transmission area in Brazil has expanded over the past decade. This expansion is thought to be linked to increased human mobility and changes in climate [7,8]. For dengue to become established in a new region, the environment must be suitable to support the propagation of the dengue vector, Aedes mosquitoes. There are two vectors present in Brazil capable of transmitting the dengue virus: Aedes aegypti and Aedes albopictus. Currently only Aedes aegypti are considered responsible for dengue transmission in Brazil [9,10], however a recent study identified Aedes albopictus infected by dengue virus in a rural area of Brazil during an outbreak, which could indicate their involvement in the introduction of dengue to rural areas [11]. Aedes aegypti have evolved to live in urban environments close to humans [12] but there is evidence to suggest they are becoming established in peri-urban and rural regions of South America [13,14]. Conversely, Aedes albopictus are typically found in peri-urban areas but have been identified in densely urbanised areas such as urban slums in Brazil [9,15]. Aedes mosquitoes breed in pools of standing, clean water created by water storage containers or uncollected refuse. These conditions arise when rapid urbanisation occurs without adequate improvements to infrastructure, such as access to piped water and refuse collection [16,17]. There is evidence that areas lacking reliable access to piped water are more susceptible to dengue outbreaks, particularly in highly urbanised areas following drought [18]. Prior studies have found that extremely wet conditions also increased the risk of dengue outbreaks, thought to be linked to the creation of larval habitat in the short term [18,19]. Suitable temperature conditions are required for the mosquitoes to breed and transmit the virus. Aedes aegypti are unable to survive in temperatures below 10°C or above 40°C [20] and can only transmit the virus between 17.8°C and 34.5°C [21,22]. Aedes albopictus are more suited to cooler temperatures and can transmit the virus between 16.2°C and 31.4°C [21,22]. Recent outbreaks in temperate cities of South America have shown that epidemics are still possible in regions that experience seasonal temperatures outside of this range due to human movement [23–25]. The expansion of Aedes aegypti and the arboviruses they transmit into rural parts of the Amazon has been linked to connections to and within the area by air, road or boat [13,26]. Despite this, the investigation of spatial connections created by human movement is little explored in the literature and the vast majority of spatial modelling studies of mosquito-borne diseases assume connectivity is based on distance alone [27]. Brazilian cities are connected to one another within a complex urban network, described within the Regions of influence of cities ("Regiões de Influência das Cidades”, REGIC) studies carried out by the Brazilian Institute of Geography and Statistics [28,29]. People often travel great distances to reach large urban centres as they contain important educational, business or cultural institutions. Failure to account for long-distance movements may miss important drivers of dengue expansion, particularly in areas such as the Amazon where the average distance travelled to Manaus, the capital of Amazonas state, was 316km. Important cities can have influence over vast areas of Brazil, for example the region of influence connected to the capital city of Brasilia corresponds to over 20% of the country and spans 1.8 million km2 [29]. Although previous studies have shown the expansion of dengue outbreaks in Brazil [7] and the association between the dengue transmission zone and climate [6], neither formally investigated the link between this expansion and human movement. In this study, we use the level of influence of cities from the REGIC studies [28,29] as a proxy for human movement, and aim to better understand how climate suitability, connectivity between cities and socioeconomic factors have contributed to the recent expansion of dengue. It is hoped that by understanding the drivers of dengue expansion in Brazil, we can identify its spatial trends and regions at risk from future outbreaks.

Discussion We found that the expansion of the dengue transmission zone is associated with temperature suitability, connectivity within the Brazilian urban network and urbanisation, and that the odds of future outbreaks significantly increase after both the vector and the virus have been introduced. This study builds on previous literature that showed the expansion of dengue across Brazil [6,7,17,26,43] and has updated the geographical barriers to transmission. The most recent epidemiological bulletins have shown that this expansion has continued in 2021 into previously unaffected parts of Acre, Amazonas, and further south into Paraná and Santa Catarina [44], highlighting the importance of monitoring the erosion of these barriers. To our knowledge, this is the first epidemiological modelling study to use the REGIC’s levels of influence and show that there is an increased odds of dengue outbreaks in cities that are highly connected within the Brazilian urban network. However, this increase is not linear; regional capitals are considered less connected than metropoles but we found that the increase in odds were higher in these cities. Further investigation is needed to understand whether this is related to human movement, as people more often travel to regional capitals from smaller cities than metropoles [29], or differences in socioeconomic factors and health-seeking behaviour that we were unable to detect at the municipality level. Although this study focuses on Brazil, there is evidence that similar patterns are emerging in other parts of South America. In Argentina, previously protected cities in temperate regions are experiencing regular outbreaks, partially related to increasing temperatures but also as a result of human movement importing cases from other parts of the continent [23,24]. Rural parts of the Amazon, which were previously isolated from infected hosts and vectors, are also experiencing outbreaks, thought to be associated with increased connectivity between rural areas and larger cities [13,17]. The introduction of dengue into Acre in the Brazilian Amazon has been linked to increased connectivity across the state following the construction of a highway between the two largest cities, Rio Branco and Cruzeiro do Sul [26]. The impact of this connection can be observed in the data as the outbreak appears to jump from Rio Branco in the south of Acre to Cruzeiro do Sul in the north in 2014 rather than spreading to neighbouring regions which appears to be the case in the South (Fig 5). The introduction of dengue into the Amazon is particularly worrying as it is the ideal environment for the virus to thrive: lower than average access to basic services such piped water and refuse collection, and the ideal climate conditions for large epidemics [17,45]. Although this study extends our understanding of the expansion of the dengue transmission zone in Brazil, there are several limitations. Dengue case data used in this study was taken from Brazil’s passive surveillance system, which has been found to differ in accuracy between regions, and between epidemic and non-epidemic periods [31]. To reduce the impact of reporting bias in our model, we used an outbreak indicator rather than case data as a response variable. The outbreak indicator used was chosen as it reflects the Brazilian Ministry of Health’s definition [37]. However, the threshold of an outbreak is likely to differ across the country. In regions that historically experienced little or no transmission, even a small number of cases may be viewed as an outbreak. The choice of such a high threshold is likely to produce more conservative estimates of the transmission zone. When our results were compared to a lower outbreak threshold of 100 cases per 100,000 residents, we found the model conclusions were consistent with the higher threshold. We found that both models using a fixed threshold outperformed the model based on the 75th percentile based on the area under the ROC curve (S7 Fig) and the Brier score. The model failed to pick up some of the temporal trends in the data, which may be a result of using stationary indicators of urbanisation and connectivity measured every 10 years. Information collected at a finer temporal scale may provide more insights into the impact of sudden expansions such as the effect of improved infrastructure in the Amazon [26]. Our model used the level of influence extracted from the REGIC studies [28,29] to account for the level of connectivity between cities within Brazil as a proxy for human movement. However, this indicator may simplify the process and miss important patterns. The hierarchical model assumed by REGIC assumes each small city is linked to a higher-level urban centre, such as the regional capitals and metropoles. It is evident that large and warm cities may propagate epidemic waves and maintain dengue transmission in their hinterland, while temperate metropoles in the South (Porto Alegre, Curitiba and São Paulo) do not play a relevant role in dengue diffusion in their region. Previous studies have found that imported cases driven by human movement are responsible for dengue outbreaks in temperate cities [24,25]. The choice of spatial connectivity assumption and data can lead to very different results and the use of the REGIC levels of influence as a spatial covariate rather than including the direct links may miss some important patterns [27]. Future work will aim to incorporate the complex urban network from the REGIC studies into a statistical framework to account for direct and indirect links between metropoles and regional capitals, and smaller urban centres in their hinterland. Despite these limitations, we have shown that the expansion of the dengue transmission zone has continued into the 21st century, driven by increased temperature suitability in the South, a network of highly connected cities, and high levels of urbanisation. The introduction of dengue outbreaks into an area more than doubles the odds of future outbreaks, which is particularly concerning given the expansion has continued into 2021. Given the dynamic nature of the growing dengue burden, the barriers identified here will be outdated very quickly. We have highlighted the importance of focusing control strategies in areas at risk of future outbreaks as well as those within the established dengue transmission zone.

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