ABSTRACT

OBJECTIVE

To present the urban arboviruses (dengue, zika and chikungunya) stratification methodology by the territorial receptivity Index, an instrument for the surveillance and control of these diseases, which considers the heterogeneity of an intra-municipal territory.

METHODS

Ecological study that uses as unit of analysis the areas covered by health centers in Belo Horizonte. For the development of a territorial receptivity index, indicators of socio-environmental determination of urban arboviruses were selected in order to integrate the analysis of main components. The resulting components were weighted by the analytic hierarchy process and combined via map algebra.

RESULTS

The territorial receptivity index showed great heterogeneity of urban infrastructure conditions. The areas classified with high and very high receptivity correspond to approximately 33% of the occupied area and are mainly concentrated in the administrative planning regions of East, Northeast, North, West, and Barreiro, especially in areas surrounding the municipality. When the density of dengue cases and Aedes eggs, from 2016, were superimposed with the stratification by the index of territorial receptivity to urban arboviruses, areas of very high receptivity had a high density of cases and Aedes eggs – higher than that observed in other areas of the city, which corresponds to a very small percentage of the municipal territory (13.5%).

CONCLUSION

The analyses indicate the need for the development of adequate surveillance and control actions for each context, overcoming the logic of homogeneous allocation throughout the territory.

Arbovirus Infections, epidemiology; Risk Factors; Risk Zone, classification; Epidemiological Monitoring; Ecological Studies

INTRODUCTION

The emergence of zika virus and chikungunya in areas of high endemicity for dengue has proved to be a great challenge for surveillance and control services in several countries. The expansion of these arboviruses in urban areas is an important public health issue, whose etiological agents are transmitted by mosquitoes of the genus Aedes , especially Aedes aegypti . With approximately 390 million cases annually in the world, such endemics results in economic and social losses, of individual and collective nature, generating increasing expenditures on clinical care¹1 Honório NA, Câmara DCP, Calvet GA, Brasil P. Chikungunya: uma arbovirose em estabelecimento e expansão no Brasil Cad Saude Publica. 2015;31(5):906-8. https://doi.org/10.1590/0102-311XPE020515
https://doi.org/10.1590/0102-311XPE02051... .

The simultaneous occurrence of the three arboviruses in Brazil is an important challenge for the Unified Health System (SUS) due to the magnitude and severity of the cases, difficulties of a differential diagnosis, and to the wide geographical distribution of cases, reaching most municipalities of the five macro-regions of the country⁵5 Ministério da Saúde (BR). Boletins Epidemiológicos. Brasília, DF; 2016 [cited 2020 Sep 9]. Available from: https://www.gov.br/saude/pt-br/assuntos/boletins-epidemiologicos
https://www.gov.br/saude/pt-br/assuntos/... .

The reproduction of these arboviruses in urban environments is conditioned by socio-environmental factors, demographic dynamics, high levels of infestation of the Aedes aegypti , and the viral circulation of different serotypes of dengue, zika, and chikungunya in each territory⁶6 Carvalho MS, Honório NA, Garcia LMT, Carvalho LCS. Aedes ægypti control in urban areas: a systemic approach to a complex dynamic. PLoS Negl Trop Dis. 2017;11(7):e0005632. https://doi.org/10.1371/journal.pntd.0005632
https://doi.org/10.1371/journal.pntd.000... , ⁷7 Donnelly MAP, Kluh S, Snyder RE, Barker CM. Quantifying sociodemographic heterogeneities in the distribution of Aedes aegypti among California households. PLoS Negl Trop Dis. 2020;14(7):e0008408. https://doi.org/10.1371/journal.pntd.0008408
https://doi.org/10.1371/journal.pntd.000... .

Historically, surveillance and entomological control actions are based on surveys on Aedes aegypti infestation indices, which, disregarding other indicators and their respective contexts, have a low capacity to predict the risk of transmission for urban arboviruses⁸8 MacCormack-Gelles B, Lima Neto AS, Sousa GS, Nascimento OJ, Castro MC. Evaluation of the usefulness of Aedes aegypti rapid larval surveys to anticipate seasonal dengue transmission between 2012-2015 in Fortaleza, Brazil. Acta Trop. 2020;205:105391. https://doi.org/10.1016/j.actatropica.2020.105391
https://doi.org/10.1016/j.actatropica.20... . Most control measures have shown a certain degree of effectiveness only when the actions are continuously applied in an intense, standardized, and wide-ranging manner⁹9 Bowman LR, Donegan S, Mccall PJ. Is dengue vector control deficient in effectiveness or evidence: systematic review and meta-analysis. PLoS Negl Trop Dis. 2016;10(3):e0004551. https://doi.org/10.1371/journal.pntd.0004551
https://doi.org/10.1371/journal.pntd.000... . Under the conditions of the municipal control services routine, none of the measures, so far, has demonstrated potential to prevent transmission in the long-term, which suggests the need for integrated and permanent approaches, capable of incorporating the territory’s socio-environmental complexity³3 Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013;496(7446):504-7. https://doi.org/10.1038/nature12060
https://doi.org/10.1038/nature12060... , ¹⁰10 Cattand P, Dejeux P, Guzmán MG, Janin J, Kroeger A, Medici A, et al. Tropical diseases lacking adequate control measures: Dengue, Leishmaniasis, and African Trypanosomiasis. In: Jamilson DT, Beman JG, Meashsam AR, Alleyne G, Claeson M, Evans DBV, et al, editors. Disease control priorities in developing countries. 2. ed. Washington, DC: The International Bank for Reconstruction and Development; New York: World Bank Publications; 2006 [cited 2020 Sep 9]. Chapter 25; p. 451-66. Available from: https://www.ncbi.nlm.nih.gov/books/NBK11753/
https://www.ncbi.nlm.nih.gov/books/NBK11... .

Given the operational limitations for vector control actions throughout a specific territory, the current strategies should be reworked, considering the heterogeneity of socio-environmental conditions and their specificities, which are fundamental for the development of specific actions for each context. Thus, the new paradigm in the control of urban arboviruses associated with Aedes aegypti maintains that the risk of transmission is distributed heterogeneously throughout the territory, which calls for approaches that stratify and qualify intra-municipal territorial units (neighborhoods, districts, administrative areas) in terms of socio-environmental conditions, proposing differentiated surveillance and control actions⁸8 MacCormack-Gelles B, Lima Neto AS, Sousa GS, Nascimento OJ, Castro MC. Evaluation of the usefulness of Aedes aegypti rapid larval surveys to anticipate seasonal dengue transmission between 2012-2015 in Fortaleza, Brazil. Acta Trop. 2020;205:105391. https://doi.org/10.1016/j.actatropica.2020.105391
https://doi.org/10.1016/j.actatropica.20... . This approach on surveillance and control is indicated by different institutions as the most suitable for the identification of areas with different levels of transmission risk¹¹11 Pan American Health Organization. Technical document for the implementation of interventions based on generic operational scenarios for Aedes aegypti control. Washington, DC: PAHO; 2019 [cited 2020 Sep 9]. Available from: https://iris.paho.org/handle/10665.2/51652
https://iris.paho.org/handle/10665.2/516... , ¹²12 World Health Organization. Handbook for integrated vector management. Geneva (CH); WHO; 2012 [cited 2020 Sep 9]. Available from: http://apps.who.int/iris/bitstream/handle/10665/44768/9789241502801_eng.pdf;jsessionid=6B69CE295A4ABE22DE977675414E596D?sequence=1
http://apps.who.int/iris/bitstream/handl... .

One research project, known as the ArboAlvo – funded by the Brazilian Ministry of Health and executed by the Oswaldo Fiocruz Institute/Oswaldo Cruz Foundation (IOC/Fiocruz) – seeks to develop risk stratification methodologies for urban arboviruses on an intra-municipal scale; thus, the method for territorial receptivity for urban arboviruses was developed.

The term “receptivity” has been used as part of the theoretical framework of studies on malaria and as a dimension of socio-environmental determinants related to the disease. This concept was expanded to the field of studies of arthropods-borne diseases in the late 1970s, from a study developed by the World Health Organization (WHO)¹³13 World Health Organization, Regional Office for Europe. Receptivity to malaria and other parasitic diseases: report on a WHO working group, Izmir, 11-15 september 1978. Copenhagen (DK); WHO Regional Office for Europe; 1978 [cited 2020 Aug 12]. Available from: https://apps.who.int/iris/handle/10665/204466
https://apps.who.int/iris/handle/10665/2... , and is still used to this day¹⁴14 World Health Organization, Regional Office for the Eastern Mediterranean. Guidelines on prevention of the reintroduction of malaria. Cairo (EG): EMRO; 2007 [cited 2020 Aug 12]. (EMRO Technical Publications Series; nº 34). Available from: https://apps.who.int/iris/handle/10665/119851
https://apps.who.int/iris/handle/10665/1... , ¹⁵15 World Health Organization. Global malaria Programme: WHO malaria terminology. Geneva (CH): WHO; 2016 [cited 2020 Aug 12]. Available from: https://apps.who.int/iris/bitstream/handle/10665/208815/WHO_HTM_GMP_2016.6_eng.pdf
https://apps.who.int/iris/bitstream/hand... . In this context, it refers to a characteristic of areas in which there is an “abundant presence of vector anophelines and the existence of other ecological and climatic factors favouring malaria transmission”¹⁴14 World Health Organization, Regional Office for the Eastern Mediterranean. Guidelines on prevention of the reintroduction of malaria. Cairo (EG): EMRO; 2007 [cited 2020 Aug 12]. (EMRO Technical Publications Series; nº 34). Available from: https://apps.who.int/iris/handle/10665/119851
https://apps.who.int/iris/handle/10665/1... . In this regard, the ecological factors involved in the concept of receptivity to malaria presuppose the existence of factors related to rural or forest territories¹⁶16 Tauil PL. Malária no Brasil: epidemiologia e controle. In: Ministério da Saúde (BR); Secretaria de Vigilância em Saúde, Departamento de Análise de Situação de Saúde. Saúde Brasil 2009: uma análise da situação de saúde e da agenda nacional e internacional de prioridades em saúde. Brasília, DF: MS; 2010. p. 223-40. (Série G. Estatística e Informação em Saúde). .

If we consider the theoretical framework initially developed for malaria and analyze the production process of vector-borne arboviruses in urban environments, such as dengue, zika, and chikungunya, we can then understand the concept of receptivity according to different socio-environmental characteristics, in relation to the infrastructural conditions that provide the reproduction of Aedes aegypti . Thus, the territorial aspects related to the urban space occupation are relevant for identifying receptivity conditions. Since they are aimed at diseases with well-established social and environmental determinants, the surveillance and control of urban arboviruses must articulate a technical component that conceives the territory as the basis for the organization of health services and actions, for population sustainability and in which the context explains the production of health problems. That is, as a field of shared responsibilities and actions, which comprises, in addition to its morphological characteristics, an area for the exercise of knowledge and power¹⁷17 Monken M, Barcellos C. Vigilância em saúde e território utilizado: possibilidades teóricas e metodológicas. Cad Saude Publica. 2005;21(3):898-906. https://doi.org/10.1590/S0102-311X2005000300024
https://doi.org/10.1590/S0102-311X200500... .

This article presents a stratification methodology via the territorial receptivity index (TRI) for urban arboviruses as a tool for the surveillance and control of dengue, zika, and chikungunya. Therefore, it considers the heterogeneity of the intra-municipal territory of Belo Horizonte, State of Minas Gerais (MG).

METHODS

The process of creating a territorial receptivity index for urban arboviruses associated with the Aedes aegypti was carried out from an ecological design that uses as unit of analysis the areas covered by health centers¹⁸18 Souza RCF, Oliveira VB, Pereira DB, Costa HSM, Caiaffa WT. Viver próximo à saúde em Belo Horizonte. Cad Metropole. 2016;18(36):325-44. https://doi.org/10.1590/2236-9996.2016-3601
https://doi.org/10.1590/2236-9996.2016-3... in Belo Horizonte. A series of indicators was synthesized in dimensions (by multivariate analysis), weighted by analytic hierarchy process (AHP)¹⁹19 Albuquerque HG, Peiter PC, Toledo LM, Alencar JAF, Sabroza PC, Dias CG, et al. Geographical information system (GIS) modeling territory receptivity to strengthen entomological surveillance: Anopheles (Nyssorhynchus) case study in Rio de Janeiro state, Brazil. Parasit Vect. 2018;11(1):256-62. https://doi.org/10.1186/s13071-018-2844-2
https://doi.org/10.1186/s13071-018-2844-... , and synthesized again, which resulted in the aforementioned index. This study was conducted within the framework of ArboAlvo, approved by the Research Ethics Committee of the Oswaldo Cruz Institute (CEP-IOC), under Protocol No. 51057015.5.0000.5537.

Area of Study

Belo Horizonte, capital of the state of Minas Gerais, has approximately 331.401 km²2 Zanluca C, Melo VC, Mosimann ALP, Santos GIV, Santos CND, Luz K. First report of autochthonous transmission of Zika virus in Brazil. Mem Inst Oswaldo Cruz. 2015;110(4):569-72. https://doi.org/10.1590/0074-02760150192
https://doi.org/10.1590/0074-02760150192... and, in 2019, an estimated urban population of 2,510,072 inhabitants, with a population density of approximately 7,167/ km²2 Zanluca C, Melo VC, Mosimann ALP, Santos GIV, Santos CND, Luz K. First report of autochthonous transmission of Zika virus in Brazil. Mem Inst Oswaldo Cruz. 2015;110(4):569-72. https://doi.org/10.1590/0074-02760150192
https://doi.org/10.1590/0074-02760150192... . The municipality is located at an average altitude of 852 meters above sea level and has high-altitude tropical climate, characterized by moderately hot and humid summers and dry winters with low temperatures. The average annual precipitation is about 1,400 mm²⁰20 Instituto Brasileiro de Geografia e Estatística. Cidades: Belo Horizonte. Rio de Janeiro: IBGE; c2017 [cited 2020 Aug 12]. Available from: https://cidades.ibge.gov.br/brasil/mg/belo-horizonte/panorama
https://cidades.ibge.gov.br/brasil/mg/be... , ²¹21 Assis WL. Os climas naturais do município de Belo Horizonte. Acta Geogr. 2012; Ed Espec:115-35. https://doi.org/10.5654/actageo2012.0002.0008
https://doi.org/10.5654/actageo2012.0002... .

In social terms, Belo Horizonte has a high Human Development Index (0.81), a moderate income distribution inequality (Gini coefficient of 0.6), and a percentage of poor population of approximately 4% (100,402 inhabitants)²⁰20 Instituto Brasileiro de Geografia e Estatística. Cidades: Belo Horizonte. Rio de Janeiro: IBGE; c2017 [cited 2020 Aug 12]. Available from: https://cidades.ibge.gov.br/brasil/mg/belo-horizonte/panorama
https://cidades.ibge.gov.br/brasil/mg/be... . The city is endemic to dengue and has reported cases of zika and chikungunya²²22 Secretaria Municipal de Saúde de Belo Horizonte. A experiência de Belo Horizonte no enfrentamento às arboviroses: dengue, zika e chikungunya. Bol Vigil Saude. 2016 [cited 2020 Aug 12];(7):1-26. Available from: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/documentos/boletim-gvsiI-arboviroses-13-1-2017.pdf
https://prefeitura.pbh.gov.br/sites/defa... .

The municipality is divided into nine administrative regions and 485 neighborhoods ( Table 1 ). In addition to the administrative planning regions (APR) and neighborhoods, the municipality of Belo Horizonte has another territorial unit, defined by the Municipal Health Department (MHD), called the health center’s area of coverage (152 areas). In the study that originated this article, the areas of coverage were used as spatial units of analysis, since the stratification of the receptivity at the intramunicipal level should be able to communicate with the territorialization of the surveillance and control actions of urban arboviruses Belo Horizonte`s MHD²³23 Barcellos C, Santos SM. Colocando dados no mapa: a escolha da unidade espacial de agregação e integração de bases de dados em saúde e ambiente através do geoprocessamento. Inf Epidemiol SUS. 1997;6(1):21-9. https://doi.org/10.5123/S0104-16731997000100003
https://doi.org/10.5123/S0104-1673199700... .

Composition of the TRI to Urban Arboviruses Associated with Aedes aegypti

From the adopted theoretical conception on territorial receptivity, 30 indicators were created based on literature review²⁴24 Flauzino RF, Souza-Santos R, Oliveira RM. Dengue, geoprocessamento e indicadores socioeconômicos e ambientais: um estudo de revisão. Rev Panam Salud Publica. 2009;25(5):456-61. and on the expertise of the authors, capable of identifying territory factors related to urban arboviruses. Indicators were elaborated regarding the municipality’s urban area growth, the population density per built area, the percentage of area with subnormal agglomerations, the altimetry, the constructed areas, the identification of vegetation areas, the conditions surrounding dwellings, and the housings sociosanitary characteristics.

For the development of Belo Horizonte’s urban growth indicator, a mapping of land use and occupancy was carried out for three years (1984, 2000, and 2017), using images from Landsat 5 and 8 (spatial resolution of 30 m) acquired via Google Engine (https://earthengine.google.com); they were analyzed by supervised classification, using the following land use classes: urban area, vegetation, exposed soil, water bodies, and roads. Finally, the percentage of urban area growth of two periods (1984–2000; 2000–2017) was calculated for each of the city’s areas of coverage.

For the identification of vegetation areas, additional mapping of land use and occupancy was carried out. Images from 2016 was used from the Pleiades satellites constellation (spatial resolution of 0.5 m), analyzed via supervised classification to identify five classes (water bodies, built-up area, exposed soil, trees, and herbaceous vegetation). We opted for images from 2016 since the index was evaluated by its relationship with the dengue occurrence data for that epidemic year.

For the development of the population density by built area indicator (hab./ km2), the denominator was estimated by the mapping of built areas, with the visual interpretation of the Pleiades satellites images from 2016. Unlike the identification of land use – in which the urban area was defined without considering the effective use by the population – this mapping delimited all areas with anthropogenic constructions, public or industrial, and excluded the green areas and incipient allotment. This process resulted in two indicators: percentage of occupied area and real population density.

The percentage of areas with subnormal clusters was obtained from the 2010 Census cartographic base. The subnormal agglomerations – often classified as favelas or other local denominations – are characterized by their difficult accessibility, high density of buildings, precarious housing, and insufficient public services, such as water supply and waste collection²⁵25 Instituto Brasileiro de Geografia e Estatística. Aglomerados subnormais. O que é? Rio de Janeiro: IBGE; 2018 [cited 2021 Jan 11]. Available from: https://www.ibge.gov.br/geociencias/organizacao-do-territorio/tipologias-do-territorio/15788-aglomerados-subnormais.html?=&t=o-que-e
https://www.ibge.gov.br/geociencias/orga... . This basis was complemented by georeferencing the information on Belo Horizonte’s favelas and by the active search for visual interpretation of satellite images. After this information collection, a base of subnormal clusters (vectorization) was built. The mapping of these areas by spatial unit of analysis resulted in the percentage of area with subnormal clusters.

The indicators for the housing’s surrounding conditions (open sewage, accumulated garbage, and lack of public lighting, paving, and manholes) and for the household conditions (water supply, sewage, garbage collection, average of people per household, source of electricity, income, and population composition), were based on the 2010 Census data. The information was combined with the adopted spatial units (areas of coverage) through the relationship between the Geographic Information Systems (GIS) plans of information.

The indicator for average altitude was created by transforming the level curves (5 m) into a smoothed surface with interpolation made by the Inverse Distance Weighted (IDW) method and subsequent mean extraction for each area of coverage via geoprocessing tools. On the other hand, the average verticalization was developed by calculating the average of the elevations of all buildings per area of coverage. Altimetry data – from laser mapping via LIDAR ( Light Detection and Ranging ) – and the level curves were obtained with the City Hall of Belo Horizonte (https://prefeitura.pbh.gov.br/prodabel).

Subsequently, statistical exploratory analysis was performed to select the indicators for the analysis of main components ( Box ), whereby three criteria were evaluated: 1) minimum variation coefficient of 25%; 2) no high positive correlation (redundancy); and 3) epidemiological plausibility. The highly negatively correlated variables were maintained by the high power of discrimination between the territorial units of analysis.

Multivariate Analysis and Calculation of the Receptivity Index

The extension of the receptivity to urban arboviruses associated with Aedes aegypti were developed from the principal components analysis (PCA), using the 21 indicators described in Box . The PCA is a multivariate analysis technique that aims to transform the original variables into components (orthogonal linear combinations) by which a synthesis is obtained with the least possible loss of information²⁶26 Jolliffe IT. Principal component analysis. 2. ed. New York: Springer International Publishing; 2002. (Springer Series in Statistics). . The indicators were standardized using the Kaiser criterion (eigenvalues > 1) and the visualization of variance decay between components (scree plot) to identify those to be selected. The importance of each main component (weight) was assessed by means of the proportion of the total variance explained by it. The loads of each indicator were used to determine their importance in the development of the component.

The Territorial Receptivity Index (TRI) was based on a multicriteria analysis²⁷27 Santos JPC, Caldas VISP, Silva AS, Santos JPC. Suscetibilidade à erosão dos solos da bacia hidrográfica lagos – São João, no Estado do Rio de Janeiro – Brasil, a partir do método AHP e análise multicritério. Rev Bras Geogr Fis. 2019;12(4):1415-30. https://doi.org/10.26848/rbgf.v12.4p1415-1430
https://doi.org/10.26848/rbgf.v12.4p1415... . This procedure involves map algebra, by which the different plans of information are crossed according to their weights and notes, resulting in the map synthesis. This integration requires the standardization of the criteria by unifying the units across all the maps²⁸28 Jiang H, Eastman JR. Application of fuzzy measures in multi-criteria evaluation in GIS. Int J Geogr Inform Sci. 2000;14():173-84. https://doi.org/10.1080/136588100240903
https://doi.org/10.1080/136588100240903... . In our study, the components used were from the PCA – such as the information plans – generating maps of receptivity with the multicriteria analysis using the method of weighted linear combination, in which the components are normalized and associated with weights obtained with the analytic hierarchy process (AHP). This method weighs each component resulting from the PCA with pairwise comparison by specialists in relation to the outcome, and then, through matrix algebra, the weight of each component is obtained. Subsequently, the TRI was divided into quintiles, so that the resulting map presents five classes (very high, high, medium, low, and very low).

To assess the relationship between the TRI and the occurrence of urban arboviruses associated with Aedes aegypti , overlappings were performed to the information plan, which included the density of dengue cases and Aedes eggs (kernel estimator) referring to the epidemic year of 2016. The statistical correlation between these variables was estimated by means of the Spearman coefficient (non-parametric), keeping the 152 areas covered by the health centers as the unit of analysis. The two overlappings of these information plans also allowed for the calculation of some indicators, such as the number of areas of coverage and average density of dengue cases and Aedes eggs according to TRI levels, with the aim of pointing out priority areas for control.

The data regarding the suspected cases of dengue reported in Belo Horizonte in 2016, georeferenced according to residential address, and the data regarding the number of eggs of Aedes collected by ovitrampas were provided by the Health Department of the municipality. Georeferenced information is available only for dengue cases, justifying the exclusive focus of this study, disregarding other urban arboviruses associated with Aedes aegypti , thus allowing for the estimation of the density of cases, which would be impossible otherwise. Moreover, the frequency of dengue cases in 2016 was predominant among all arboviruses (154,143 cases or 99%) in relation to zika (1,495 cases or 0.1%) and chikungunya (95 cases or 0.01%), so that the exclusion of these two arboviruses does not affect the evaluation of the relationship between the index and the occurrence of dengue cases²²22 Secretaria Municipal de Saúde de Belo Horizonte. A experiência de Belo Horizonte no enfrentamento às arboviroses: dengue, zika e chikungunya. Bol Vigil Saude. 2016 [cited 2020 Aug 12];(7):1-26. Available from: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/documentos/boletim-gvsiI-arboviroses-13-1-2017.pdf
https://prefeitura.pbh.gov.br/sites/defa... .

RESULTS

The spatial exploratory analysis of the selected indicators points to a recent process of urban expansion directed to the northeast and northwest portions of the city, as well as to the occurrence of a territorial heterogeneity of socioeconomic conditions, housing infrastructure, and housing environment. Figure 1 shows, among the pre-selected indicators, those with greater epidemiological plausibility in the socio-environmental determination process and territorial variability.

Based on the PCA result, we chose to work with the first four components generated by the analysis, which together explain approximately 61% of the observed variance. These components were spatialized and interpreted based on the municipal territory knowledge ( Figure 2 ).

The first resulting component, which explains approximately 29% of the variability of the data set, was defined as peripheral areas of population and poverty concentration with urban infrastructure deficiency and low percentage of white people. Thus, areas with high value of this component have a high percentage of households with a monthly income per capita of up to one minimum wage, without pavement in the surroundings, and with water supply by well, rainwater stored in cisterns and / or other form of water supply.

The second component, defined as concentrated poverty in consolidated urban area, explains approximately 15% of the variability. In the spatial units of analysis in which the value of this component is high, it is observed: a higher density in population and poor people, higher percentage of housings as irregular occupation, and higher percentage of favela areas, that is, in subnormal agglomerations.

The third component explains approximately 10% of the variability of the data set and was defined as areas with high altitudes and high verticalization with heterogeneity of urban infrastructure. The fourth component has an explanation percentage of approximately 7% and designates a dense area with urban precariousness. In the areas with high value for this last component there is high population density, high percentage of housings in irregular occupation, high percentage of housings with accumulated garbage and with open sewage in the surroundings.

The weighting process of these components for the elaboration of the index through the AHP resulted in the following weights: 17.4% for the first; 34% for the second; 7.2% for the third; and 41.4% for the fourth. Based on these weights and through the map algebra technique, we obtained the TRI for each of the units of analysis. The index was spatialized with the areas of coverage of the basic health units, classified into five categories of receptivity: very low; low; average; high; and very high ( Figure 3 ).

The areas classified as high and very high receptivity, corresponding to approximately 33% of the occupied area of the municipality ( Table 2 ), are mainly concentrated in the administrative planning regions (APR) of East, Northeast, North, West, and Barreiro, mainly in areas bordering other municipalities that make up the Metropolitan Region. However, the presence of areas classified as such is observed in all APR of the city. The areas classified as low or very low receptivity, on the other hand, are concentrated in the Central-South and Pampulha APR, characterized by the occupation of people with average and high incomes and by a good network of services and urban infrastructure. These areas correspond to about 52% of the occupied area of the municipality ( Table 2 ).

When overlapping the density of dengue cases and Aedes eggs, from 2016, with the stratification by TRI classes to urban arboviruses, it is found that areas of very high receptivity have a certain density of cases, as well as higher amounts of Aedes eggs than that observed in the other areas of the city, which correspond to a very small percentage of the municipal territory (13.5%) ( Figure 3 , Table 2 ). Spearman’s correlation coefficient between TRI and dengue case density was 0.45 (p-value < 0.05; 95%CI: 0.27–0.53). For the correlation between receptivity and Aedes egg density, the value was 0.06 (p-value = 0.43). Although in the latter case the Spearman correlation is not significant, we emphasize that this analysis observes the existence of a linear relationship between the TRI and the density of Aedes eggs for each space unit. When we observe the relationship according to the TRI classes, we can verify higher density of Aedes eggs in the classes of higher receptivity.

DISCUSSION

The proposition and elaboration of a TRI to urban arboviruses associated with the Aedes aegypti was able to show intra-municipal heterogeneity regarding the infrastructure conditions of Belo Horizonte. The analyses highlight the need for the development of particular surveillance and control actions to each context, in order to overcome the logic of homogeneous allocation of actions throughout the territory.

The results here presented show the territorial characteristics in the scale of area of coverage (spatial unit used). This perspective makes visible some patterns of the distribution of living conditions and infrastructure of the territories but does not fully cover the phenomenon complexity. Had this study been conducted on another scale, the analysis would naturally present other results, which would enrich the understanding of the territorial context in which urban arboviruses occur²⁹29 Machado JP, Oliveira RM, Souza-Santos R. Análise espacial da ocorrência de dengue e condições de vida na cidade de Nova Iguaçu, Estado do Rio de Janeiro, Brasil. Cad Saude Publica. 2009;25(5):1025-34. https://doi.org/10.1590/S0102-311X2009000500009
https://doi.org/10.1590/S0102-311X200900... .

Since the TRI indicates areas more receptive to urban arboviruses associated with Aedes aegypti , depending on the organization and use of the territory, it is not primarily directed to deal with epidemic emergencies; however, in the absence of a more qualified information in a scenario such as this, the receptivity index can serve as a parameter for the allocation of surveillance and control actions in the territory.

Considering situations of explosive epidemics, indicative of high susceptibility in the population, such as the one that occurred in Belo Horizonte in 2016, with significant circulation of DENV1 serotype and an abrupt rise of the case notification curve with high levels maintained over several epidemiological weeks²²22 Secretaria Municipal de Saúde de Belo Horizonte. A experiência de Belo Horizonte no enfrentamento às arboviroses: dengue, zika e chikungunya. Bol Vigil Saude. 2016 [cited 2020 Aug 12];(7):1-26. Available from: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/documentos/boletim-gvsiI-arboviroses-13-1-2017.pdf
https://prefeitura.pbh.gov.br/sites/defa... , we observed in our study a higher density of dengue cases in spatial units classified as high or very high receptivity, which suggests the usefulness of this index as a predictor of risk areas for these situations. Additionally, the overlapping of Aedes egg density observed in that epidemic year with the stratification by the TRI indicated a similar result to that observed for the density of cases. However, we emphasize the need for TRI analysis in other cities and other epidemic years.

Therefore, this tool aims to strengthen the SUS, helping with the structural planning of local surveillance and control programs against urban arboviruses associated with the Aedes aegypti, indicating the portions of the city in which, in a general and systematic way, more intense actions are needed⁸8 MacCormack-Gelles B, Lima Neto AS, Sousa GS, Nascimento OJ, Castro MC. Evaluation of the usefulness of Aedes aegypti rapid larval surveys to anticipate seasonal dengue transmission between 2012-2015 in Fortaleza, Brazil. Acta Trop. 2020;205:105391. https://doi.org/10.1016/j.actatropica.2020.105391
https://doi.org/10.1016/j.actatropica.20... , ¹¹11 Pan American Health Organization. Technical document for the implementation of interventions based on generic operational scenarios for Aedes aegypti control. Washington, DC: PAHO; 2019 [cited 2020 Sep 9]. Available from: https://iris.paho.org/handle/10665.2/51652
https://iris.paho.org/handle/10665.2/516... . In this sense, considering the context of lack of human resources, one of the possible applications of TRI by local managers would be to subsidize the organization of control actions prioritizing areas with greater receptivity.

Moreover, we believe that the TRI is a strategic tool for intersectoral dialogue within the public administration, since it expresses the heterogeneity of territorial occupation and the quality of urban infrastructure and services in their relations with the potential occurrence of cases of arboviruses; thus, highlighting the need for changes in these socio-technical infrastructures, whose competencies go beyond individual ones, within the healthcare sector³⁰30 World Health Organization. The 8. Global Conference on Health Promotion; 10-14 June 2013; Helsinki, Finland. Geneva (CH): WHO; 2013 [cited 2020 Aug 18]. Available from: https://www.who.int/healthpromotion/conferences/8gchp/8gchp_helsinki_statement.pdf
https://www.who.int/healthpromotion/conf... .

In relation to its elaboration process, the strengths of the study are in the availability of sociodemographic and environmental data available in free databases that are accessible via the internet, as well as the possibility of being applied to other cities. In this sense, it is still important to emphasize that the technical procedures to which these data are submitted can be carried out in free computer programs, easy to obtain and install. As necessary resources for its elaboration, professionals are needed to perform the territorial analysis in health, as well as secondary data and spatial analysis. We emphasize, thus, the importance of regularly carrying out training processes for the improvement of the technical capacities of professionals for the surveillance of urban arboviruses.

Regarding the TRI index, we note as a great advantage the fact that it can synthesize the complex socio-environmental determinants for the occurrence of urban arboviruses (as demonstrated by the overlap of the density of dengue cases and Aedes eggs by this index) into an easily understandable and communicable numerical value. This index successfully answers the question posed by Machado et al.²⁸28 Jiang H, Eastman JR. Application of fuzzy measures in multi-criteria evaluation in GIS. Int J Geogr Inform Sci. 2000;14():173-84. https://doi.org/10.1080/136588100240903
https://doi.org/10.1080/136588100240903... on the importance of the development of composite indicators capable of combining different dimensions of the territory and, thus, encompassing the set of socio-environmental characteristics that determine the production and reproduction of urban arboviruses. In this sense, the Municipal Council of Belo Horizonte had already developed the health vulnerability index (IVS-BH), a composite indicator that synthesizes socioeconomic variables to differentiate areas with unfavorable conditions in the intra-urban space³¹31 Secretaria Municipal de Saúde de Belo Horizonte. Índice de vulnerabilidade da saúde. Belo Horizonte, MG; 2012 [cited 2020 Aug 12]. Available from: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/publicacaoes-da-vigilancia-em-saude/indice_vulnerabilidade2012.pdf
https://prefeitura.pbh.gov.br/sites/defa... . Although the IVS-BH is an important tool to guide public health policies and prioritize resource allocation, we note the need for a composite indicator specifically related to the socio-environmental determinants of urban arboviruses associated with the Aedes aegypti . Thus, the TRI uses more specific census indicators, as well as climate and territorial information from remote sensing.

Finally, as a development perspective in the characterization of territorial receptivity to urban arboviruses associated with the Aedes aegypti, we highlight the importance of incorporating indicators that reflect the dynamics and conjunctions of the territories, in the spatial and temporal perspectives, since the territory is constantly changing due to the dynamics that reflect the modeling flows of geographical space³²32 Santos M. A natureza do espaço: técnica e tempo, razão e emoção. 4.ed. São Paulo: Editora da Universidade de São Paulo; 2006. (Coleção Milton Santos; nº 1). .

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