Abstract

Introduction

Nowadays, dengue is the most prevalent arthropod-borne virosis in the world, with approximately 40% of the population at risk¹1. da Silva-Voorham JM, Tami A, Juliana AE, Rodenhuis-Zybert IA, Wilschut JC, Smit JM. Dengue: a growing risk to travellers to tropical and sub-tropical regions. Ned Tijdschr Geneeskd 2009; 153: A778.. Four serotypes of the virus circulate, significantly increasing the severe and lethal forms of the disease²2. Pinheiro FP, Corber SJ. Global situation of dengue and dengue haemorrhagic fever, and its emergence in the Americas. World Health Stat Q 1997; 50(3-4): 161-9. ^{, 3}3. Wilder-Smith A, Chen LH, Massad E, Wilson ME. Threat of dengue to blood safety in dengue-endemic countries . Emerg Infect Dis 2009; 15(1): 8-11..

The number of cases of classic dengue and of dengue hemorrhagic fever has been increasing on an annual basis. It is estimated that 550 thousand hospitalizations with 20 thousand deaths occur per year among a total of approximately 2.5 billion exposed people⁴4. World Health Organization. Report of the Scientific Working Group meeting on Dengue . Geneva; 2006. ^{, 5}5. World Health Organization. WHO report on global surveillance of epidemic-prone infectious diseases. Geneva; 2000.,and an average of 80 million new cases are reported every year²2. Pinheiro FP, Corber SJ. Global situation of dengue and dengue haemorrhagic fever, and its emergence in the Americas. World Health Stat Q 1997; 50(3-4): 161-9..

As a reemerging endemic or pandemic disease, it occurs practically in all the tropical and subtropical regions of the planet¹1. da Silva-Voorham JM, Tami A, Juliana AE, Rodenhuis-Zybert IA, Wilschut JC, Smit JM. Dengue: a growing risk to travellers to tropical and sub-tropical regions. Ned Tijdschr Geneeskd 2009; 153: A778.. The countries located in these regions are more susceptible due to diverse conditioning factors, such as: global changes, climate changes, weather variability, land use, water storage and irrigation, human population growth and urbanization⁶6. Sutherst RW. Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev 2004; 17(1): 136-73.. Such factors, among others, significantly contribute to the proliferation and development of the Aedes aegypti mosquito – the virus vector ^7-9. Climate changes contribute to increase the number of people exposed to dengue to more than 2 billion and the projections for 2085 suggest that approximately 5 to 6 billion people (50 to 60% of the world's population) will be at risk regarding the disease transmission¹⁰10. Hales S, de Wet N, Maindonald J, Woodward A. Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet 2002; 36(9336): 830-4..

The seasonal dynamics of the dengue vector is commonly associated with climate changes and fluctuations⁹9. Ribeiro AF, Marques GR, Voltolini JC, Condino ML. Associação entre incidência de dengue e variáveis climáticas. Rev Saúde Pública 2006; 40(4): 671-6. ^{, 11}11. Hemmer CJ, Frimmel S, Kinzelbach R, Gürtler L, Reisinger EC. Global warming: trailblazer for tropical infections in Germany? Dtsch Med Wochenschr 2007; 132(48): 2583-9., which include: temperature increase and variations in rainfall and relative air humidity, conditions that favor a higher number of available breeding sites and, consequently, the development of the vector. The latter presents two distinct stages: aquatic, with the development phases of egg, larva and pupa, and terrestrial, which corresponds to the adult mosquito. Both stages are subject to environmental and climate changes¹²12. Campbell-Lendrum D, Corvalán C. Climate Change and Developing-Country Cities: Implications For Environmental Health and Equity. J Urban Health 2007; 84(S1): 109-17. ^{, 13}13. Tabachnick WJ. Challenges in predicting climate and environmental effects on vector-borne disease episystems in a changing world. J Exp Biol 2010; 213(6): 946-54..

In Brazil, the introduction of laboratory testing for dengue dates back to 1981-1982, in the city of Boa Vista, State of Roraima – in the Brazilian Amazon -, where the serotypes DENV-1 and 4 were isolated, with 11,000 confirmed cases¹⁴14. Osanai CH, Travassos da Rosa AP, Tang AT, do Amaral RS, Passos AD, Tauil PL. Surto de dengue em Boa Vista, Roraima Nota previa. Rev Inst Med Trop Sâo Paulo 1983; 25(1): 53-4.. Since then, the country has undergone several epidemic outbreaks¹⁵15. Schatzmayr HG. Dengue situation in Brazil by year 2000. Mem Inst Oswaldo Cruz 2000; 95 (S1): 179-81. ^{, 16}16. Schatzmayr HG, Nogueira RMR, Travassos da Rosa AP. An outbreak of dengue virus at Rio de Janeiro - 1986. Mem Inst Oswaldo Cruz 1986; 81(2): 245-6..

Ae. Aegypti dispersal currently reaches the 27 Brazilian Federative Units, with more than 3,587 cities infested with the disease vector. In recent decades, dengue has become an important cause of morbidity and mortality¹⁷17. Brasil. Fundação Nacional de Saúde. Centro Nacional de Epidemiologia. Boletim eletrônico epidemiológico . Brasília; 2001. ^{, 18}18. Brasil. Ministério da Saúde. Informe Epidemiológico da Dengue/Análise de situação e tendências . Brasília; 2010..

Brazil is considered a tropical country because it is located at low latitude zones, in which hot and humid climates prevail, with average temperatures around 20ºC¹⁹. With an area of 8.5 million km², the country is formed by five geographical regions (North, Northeast, Center-West, Southeast and South) and five climate zones: Equatorial, Temperate, Central Brazil Tropical, Eastern Northeast Tropical and Equatorial Zone Tropical²⁰20. Instituto Brasileiro de Geografia e Estatística [homepage na internet]. Brasília: Ministério do Planejamento, Orçamento e Gestão; 2005. Disponível em: http://mapas.ibge.gov.br/clima/ viewer.htm (Acessado em 28 de fevereiro de 2012).
http://mapas.ibge.gov.br/clima/ viewer.h... .

Brazil's climate variability is due to the territory's dimension, the size of the coastal strip, altitude variation and, mainly, to the presence of different air masses that modify the temperature and humidity conditions of the five regions. For this reason, the country's climate ranges from hot, super-humid climates deriving from equatorial air masses, as it is the case of a large part of the Amazon region, to semi-arid climates, typical of the Northeastern backlands²⁰20. Instituto Brasileiro de Geografia e Estatística [homepage na internet]. Brasília: Ministério do Planejamento, Orçamento e Gestão; 2005. Disponível em: http://mapas.ibge.gov.br/clima/ viewer.htm (Acessado em 28 de fevereiro de 2012).
http://mapas.ibge.gov.br/clima/ viewer.h... ^{, 21}21. Mendonça FA, Danni-Oliveira IM. Climatologia - Noções básicas e climas do Brasil . São Paulo: Oficina de textos; 2007..

Considering the diverse studies that show the relation between environmental determinants and climate factors under the dynamics of endemics, and in view of the pertinence and magnitude of dengue in Brazil and in the world, the development of a literature review becomes relevant. This study aims to present a systematic review of the Brazilian scientific literature on the occurrence of dengue and its relationship to climate variables.

Methodology

Study design

This study is a systematic bibliographic review carried out in different scientific electronic databases, using descriptors referring to dengue and climate variables in Brazil. The identification of the papers and their inclusion occurred in the first semester of 2010.

Electronic databases

The bibliographical survey was conducted in the following electronic databases: Scientific Electronic Library Online - SciELO; (2) Medical Literature Analysis and Retrieved System - MEDLINE; (3) Literatura Latino-americana e do Caribe em Ciências da Saúde - Lilacs; (4) U.S. National Library of Medicine - PubMed.

Complementary information was obtained from epidemiological bulletins; reports on climate and environmental changes published by the World Health Organization (WHO), Pan-American Health Organization (PAHO) and Brazil's Ministry of Health; geographical and climate data provided by the Instituto Brasileiro de Geografia e Estatística (IBGE – Brazilian Institute of Geography and Statistics). A manual search was also performed, based on the references listed in the papers that were included in the review.

Search strategies

The searches were performed through descriptors registered in the Descritor em Ciências da Saúde (DeCS - Health Sciences Descriptor) and in the Medical Subject Headings – MeSH, in Portuguese and in English, which were present in the studies' titles or abstracts. To facilitate the search, the Boolean operators “AND” and “OR” were used, as well as quotation marks.

The combinations of terms used together or separately in the respective databases (SciELO, PubMed, Medline, LILACS) were:

• ·

  “Dengue (dengue)”;

• ·

  “ Aedes ( Aedes )”;

• ·

  “Dengue variáveis meteorológicas (dengue meteorological variables)”;

• ·

  “Dengue fatores climáticos (dengue climatic factors)”;

• ·

  “Dengue temperatura (dengue temperature)”;

• ·

  “Dengue umidade (dengue humidity)”;

• ·

  “Dengue verão (dengue summer)”;

• ·

  Dengue chuva (dengue rain);

• ·

  “Dengue inverno (dengue winter)”;

• ·

  Dengue pluviosidade (dengue rainfall)”.

Selection and analysis of publications

To select the papers, a form was constructed with the following information: author and year, journal, title, period of development of the study, federative unit, city and area of the research, study design, inclusion in databases, descriptor used to locate the paper, statistical analysis method, objective and main results.

The inclusion criteria were: original papers published in international or national journals, in English, Portuguese or Spanish, independently of the year of publication, included in one of the databases mentioned above.

Only papers that contained analyses of meteorological variables and the relationship to the occurrence of dengue in Brazil were selected to the review. Studies that used Aedes aegypti as the main transmission vector, as well as Aedes albopictus , among others of lower prevalence, were included.

Overall, 625 scientific papers relating dengue to environmental/meteorological factors in Brazil and in the world were identified. Of the total of 43 papers that were produced with Brazilian data, 12 studies were excluded, either because they were not related to the review's theme or because they were duplicated. Thus, 31 papers were selected to be included in this scientific literature review. The results obtained through the application of the search strategy that was described above are shown in the study's logical framework.

The studies are presented in maps by Federative Units, geographical regions and according to the country's climate zones. In addition, they are presented in a table according to publication chronology, climate, place of study, meteorological variables and main findings. The results and discussion are presented below, divided into rainfall, rainfall/temperature, temperature/relative air humidity, and lag.

Results and discussion

Reviewed papers

Of the overall number of 31 (thirty-one) original and distinct papers included in the review, 12 (twelve) publications concentrate on temperature (^oC) and rainfall (mm); 9 (nine) approach rainfall; 7 (seven) papers focus on temperature, rainfall, atmospheric pressure, wind direction and relative air humidity; 1 (one) study mentioned the abiotic factor quarterly and semi-annual temperature of each year; 1 (one) study compared distinct rain and drought periods; 1 (one) publication referred to summer/winter seasonal differentiation in relation to the incidence of dengue ( Figure 1 ).

It was found that all the studies used quantitative approaches, and that the main methods employed in the studies were: capturing mosquitoes through traps (ovitraps, mosquiTRAPs, vacuums, baits, among other methods); entomological/larval surveys in reservoirs, tanks, vats, vases, tires; entomological survey in buildings by means of the Breteau index and the building infestation index – BII. The most frequent were the cross-sectional epidemiological studies and also the ecological, descriptive, time-series studies, which used secondary data of the Sistema Nacional de Agravos de Notificação (SINAN – National Notifiable Diseases Database) and spatial analyses. Among the employed types of analyses, the highlights are correlations and geoprocessing techniques, especially through the Kernel method.

Distribution of the studies

Figures 2 and 3 show the number of publications according to areas of study by Federative Units, geographical regions and in conformity with the country's climate zones. Figure 2 shows that the largest number of studies was conducted in the State of São Paulo, SP, followed by Rio de Janeiro, RJ. Studies were published about the entire Southeast region, except for the State of Espírito Santo. On the other hand, only one study was published about the South region, conducted in a city of the State of Paraná. Figure 3 shows the number of studies published by climate zones. It can be seen that studies were carried out in areas that are affected by the five Brazilian climates. Studies relating dengue to meteorological variables were more frequent in areas of the Central Brazil Tropical Climate.

Table 1 presents, in chronological order and by climate, the studies on the theme of dengue and meteorological variations in Brazil that were published between 1992 and 2010. In terms of temporal evolution, the highest number of publications occurred from the year 2000 onwards.

Rainfall

The abiotic factor rain²²22. Gomes Ade C, Forattini OP, Kakitani I, Marques GR, Marques CC, Marucci D et al. Microhabitats de Aedes albopictus (Skuse) na região do Vale do Paraíba, Estado de São Paulo, Brasil. Rev Saude Publica 1992; 26(2): 108-18.

23. Chiaravalloti Neto F. Descrição da colonização de Aedes aegypti na região de São José do Rio Preto, São Paulo. Rev Soc Bras Med Trop 1997; 30(4): 279-85.

24. Rebêlo JM, Costa JM, Silva FS, Pereira YN, da Silva JM. Distribuição de Aedes aegypti e do dengue no Estado do Maranhão, Brasil. Cad Saúde Pública 1999; 15(3): 477-86.

25. Forattini OP, Kakitani I, dos Santos RLC, Kobayashi KM, Ueno HM, Fernandez Z. Comportamento de Aedes albopictus e Ae. scapularis adultos (Diptera: Culicidae) no sudeste do Brasil. Rev Saúde Pública 2000; 34(5): 461-7.

26. Pinheiro VC, Tadei WP. Frequency, diversity, and productivity study on the Aedes aegypti most preferred containers in the city of Manaus, Amazonas, Brazil. Rev Inst Med Trop Sao Paulo 2002; 44(5): 245-50.

27. Souza IC, Vianna RP, Moraes RM. Modelagem da incidência do dengue na Paraíba, Brasil, por modelos de defasagem distribuída. Cad Saúde Pública 2007; 23(11): 2623-30.

28. Costa FS, Silva JJ, Souza CM, Mendes J. Dinâmica populacional de Aedes aegypti (L) em área urbana de alta incidência de dengue. Rev Soc Bras Med Trop 2008; 41(3): 309-12. ^{- 29}29. Zeidler JD, Acosta PO, Barrêto PP, Cordeiro Jda D. Dengue virus in Aedes aegypti larvae and infestation dynamics in Roraima, Brazil. Rev Saude Publica 2008; 42(6): 986-91.was important for the production of larvae, pupae and occurrence of dengue. The infestations occurred mainly in the months of highest rainfall levels at the different areas. Studies carried out in Vale do Paraíba (SP)²², São José do Rio Preto (SP)²³23. Chiaravalloti Neto F. Descrição da colonização de Aedes aegypti na região de São José do Rio Preto, São Paulo. Rev Soc Bras Med Trop 1997; 30(4): 279-85., in the state of Maranhão (MA)²⁴24. Rebêlo JM, Costa JM, Silva FS, Pereira YN, da Silva JM. Distribuição de Aedes aegypti e do dengue no Estado do Maranhão, Brasil. Cad Saúde Pública 1999; 15(3): 477-86., Vila das Pedrinhas (south coast of the state of São Paulo)²⁵25. Forattini OP, Kakitani I, dos Santos RLC, Kobayashi KM, Ueno HM, Fernandez Z. Comportamento de Aedes albopictus e Ae. scapularis adultos (Diptera: Culicidae) no sudeste do Brasil. Rev Saúde Pública 2000; 34(5): 461-7., Manaus (AM)²⁶26. Pinheiro VC, Tadei WP. Frequency, diversity, and productivity study on the Aedes aegypti most preferred containers in the city of Manaus, Amazonas, Brazil. Rev Inst Med Trop Sao Paulo 2002; 44(5): 245-50., Paraíba (PB)²⁷27. Souza IC, Vianna RP, Moraes RM. Modelagem da incidência do dengue na Paraíba, Brasil, por modelos de defasagem distribuída. Cad Saúde Pública 2007; 23(11): 2623-30., Uberlândia (MG)²⁸28. Costa FS, Silva JJ, Souza CM, Mendes J. Dinâmica populacional de Aedes aegypti (L) em área urbana de alta incidência de dengue. Rev Soc Bras Med Trop 2008; 41(3): 309-12.and Boa Vista (RR)²⁹29. Zeidler JD, Acosta PO, Barrêto PP, Cordeiro Jda D. Dengue virus in Aedes aegypti larvae and infestation dynamics in Roraima, Brazil. Rev Saude Publica 2008; 42(6): 986-91.have shown that, even though there are differences in the rain dynamics in the several regions of Brazil, the highest incidence of the disease and the highest levels of vector infestations coincided with the rainy months, which were also the hottest months of the year in the country³⁰30. Câmara FP, Theophilo RL, dos Santos GT, Pereira SR, Câmara DC, de Matos RR. Estudo retrospectivo (histórico) da dengue no Brasil: características regionais e dinâmicas. Rev Soc Bras Med Trop 2007; 40(2): 192-6..

A study conducted in all the 246 cities of the state of Goiás³¹31. Souza SS, Silva IG, Silva HHG. Associação entre incidência de dengue, pluviosidade e densidade larvária de Aedes aegypti , no Estado de Goiás. Rev Soc Bras Med Trop 2010; 43(2): 152-5.(Central-Western Brazil) from January 2001 to December 2005 showed that the building infestation index (BII) concerning Ae. Aegypti presented an important variability over the months, and also that there is a significant association between the peaks of the disease and periods of high BII and medium rainfall levels. Larval density and the number of dengue cases increased during the first four months of each year (period of high rainfall levels) and decreased between June and September (lower rainfall levels). These results were also found in studies conducted in São José do Rio Preto (SP)²³, Maranhão (MA)²⁴24. Rebêlo JM, Costa JM, Silva FS, Pereira YN, da Silva JM. Distribuição de Aedes aegypti e do dengue no Estado do Maranhão, Brasil. Cad Saúde Pública 1999; 15(3): 477-86., Vila das Pedrinhas (SP)²⁵25. Forattini OP, Kakitani I, dos Santos RLC, Kobayashi KM, Ueno HM, Fernandez Z. Comportamento de Aedes albopictus e Ae. scapularis adultos (Diptera: Culicidae) no sudeste do Brasil. Rev Saúde Pública 2000; 34(5): 461-7.and Tupã (SP)³²32. Barbosa GL, Lourenço RW. Análise da distribuição espaço-temporal de dengue e da infestação larvária no município de Tupã, Estado de São Paulo. Rev Soc Bras Med Trop 2010; 43(2): 145-51..

The climate of the state of Goiás is Central Brazil Tropical, with two well-defined seasons: extremely dry in the middle of the year and rainy in the summer, with a period of drought that lasts from 5 to 6 months (May to September) and a rainy season that lasts from October to April³¹31. Souza SS, Silva IG, Silva HHG. Associação entre incidência de dengue, pluviosidade e densidade larvária de Aedes aegypti , no Estado de Goiás. Rev Soc Bras Med Trop 2010; 43(2): 152-5.. The climate of Goiás is similar to the climate of the other states located in the Central-West region and the cycles of rainfall seasonality are similar to those of the rest of Brazil, except for some regions of the Northeast, which have the Eastern Northeast Tropical climate, and of the Northern Amazon, which have the Equatorial Zone Tropical Climate²⁰20. Instituto Brasileiro de Geografia e Estatística [homepage na internet]. Brasília: Ministério do Planejamento, Orçamento e Gestão; 2005. Disponível em: http://mapas.ibge.gov.br/clima/ viewer.htm (Acessado em 28 de fevereiro de 2012).
http://mapas.ibge.gov.br/clima/ viewer.h... ^{, 21}21. Mendonça FA, Danni-Oliveira IM. Climatologia - Noções básicas e climas do Brasil . São Paulo: Oficina de textos; 2007..

There are studies that show the incidence rate of the disease by seasons. In Manaus, a lower incidence of dengue was verified in the dry season, when the Ae. Aegypti mosquito was found in 84-90% of the houses, while the highest values were verified in November (transition/rainy period), with 94-98% of positive households³³33. Ríos-Velásquez CM, Codeço CT, Honório NA, Sabroza PS, Moresco M, Cunha IC et al. Distribution of dengue vectors in neighborhoods with different urbanization types of Manaus, state of Amazonas, Brazil. Mem Inst Oswaldo Cruz 2007; 102(5): 617-23.. It is known that, in Manaus, the predominant climate is the Equatorial one²⁰20. Instituto Brasileiro de Geografia e Estatística [homepage na internet]. Brasília: Ministério do Planejamento, Orçamento e Gestão; 2005. Disponível em: http://mapas.ibge.gov.br/clima/ viewer.htm (Acessado em 28 de fevereiro de 2012).
http://mapas.ibge.gov.br/clima/ viewer.h... , with the rainy season lasting from January to May and the dry season, from July to September³³33. Ríos-Velásquez CM, Codeço CT, Honório NA, Sabroza PS, Moresco M, Cunha IC et al. Distribution of dengue vectors in neighborhoods with different urbanization types of Manaus, state of Amazonas, Brazil. Mem Inst Oswaldo Cruz 2007; 102(5): 617-23..

A study carried out in 2005³⁴34. Maciel-de-Freitas R, Peres RC, Souza-Santos R, Lourenço-de-Oliveira R. Occurrence, productivity and spatial distribution of key-premises in two dengue-endemic areas of Rio de Janeiro and their role in adult Aedes aegypti spatial infestation pattern. Trop Med Int Health 2008; 13(12): 1488-94.in the city of Rio de Janeiro showed that there was no statistically significant difference in infestation between the two periods, and the seasonality effect was described as being low or absent in the majority of the reservoirs analyzed in that city. Honório et al.³⁵35. Honório NA, Codeço CT, Alves FC, Magalhães MA, Lourenço-De-Oliveira R. Temporal distribution of Aedes aegypti in different districts of Rio de Janeiro, Brazil, measured by two types of traps. J Med Entomol 2009; 46(5): 1001-14., in a study that was also conducted in Rio de Janeiro about the temporal distribution of Ae. Aegypti between September 2006 and March 2008, found an important association with positive ovitraps. In the summer, the average indexes were of 70-80%, reaching expressive peaks of 90-100%, while in the winter, the infestation suffered a reduction, but it rarely remained below 60%, which shows that the mosquito is prevalent all year long. The largest abundance was found in the hottest and most humid period of the year, indicating seasonality³⁵35. Honório NA, Codeço CT, Alves FC, Magalhães MA, Lourenço-De-Oliveira R. Temporal distribution of Aedes aegypti in different districts of Rio de Janeiro, Brazil, measured by two types of traps. J Med Entomol 2009; 46(5): 1001-14.. Rio de Janeiro has the Central Brazil Tropical climate²⁰20. Instituto Brasileiro de Geografia e Estatística [homepage na internet]. Brasília: Ministério do Planejamento, Orçamento e Gestão; 2005. Disponível em: http://mapas.ibge.gov.br/clima/ viewer.htm (Acessado em 28 de fevereiro de 2012).
http://mapas.ibge.gov.br/clima/ viewer.h... and its temperature varies between 20ºC and 27ºC. The hottest months occur between November and April, and the coldest, between May and October. Rain is most frequent between December and March (January is the rainiest month), and the driest period occurs from June to September³⁶36. Câmara FP, Gomes AF, Santos GT, Câmara DC. Clima e epidemias de dengue no Estado do Rio de Janeiro. Rev Soc Bras Med Trop 2009; 42(2): 137-40., similarly to the majority of the Brazilian states.

Many studies that employed entomological surveys²²22. Gomes Ade C, Forattini OP, Kakitani I, Marques GR, Marques CC, Marucci D et al. Microhabitats de Aedes albopictus (Skuse) na região do Vale do Paraíba, Estado de São Paulo, Brasil. Rev Saude Publica 1992; 26(2): 108-18. ^{, 23}23. Chiaravalloti Neto F. Descrição da colonização de Aedes aegypti na região de São José do Rio Preto, São Paulo. Rev Soc Bras Med Trop 1997; 30(4): 279-85. ^{, 26}26. Pinheiro VC, Tadei WP. Frequency, diversity, and productivity study on the Aedes aegypti most preferred containers in the city of Manaus, Amazonas, Brazil. Rev Inst Med Trop Sao Paulo 2002; 44(5): 245-50. ^{, 29}29. Zeidler JD, Acosta PO, Barrêto PP, Cordeiro Jda D. Dengue virus in Aedes aegypti larvae and infestation dynamics in Roraima, Brazil. Rev Saude Publica 2008; 42(6): 986-91. ^{, 37}37. Honório NA, Cabello PH, Codeço CT, Lourenço-de-Oliveira R. Preliminary data on the performance of Aedes aegypti and Aedes albopictus immatures developing in water-filled tires in Rio de Janeiro. Mem Inst Oswaldo Cruz 2006; 101(2): 225-8.

38. Forattini OP, Kakitani I, Ueno HM. Emergência de Aedes albopictus em recipientes artificiais. Rev Saude Publica 2001; 35(5): 456-60. ^{- 39}39. Favier C, Degallier N, Vilarinhos PT, de Carvalho MS, Yoshizawa MA, Knox MB. Effects of climate and different management strategies on Aedes aegypti breeding sites: a longitudinal survey in Brasília (DF, Brazil). Trop Med Int Health 2006; 11(7): 1104-18.have shown higher values of infestation of eggs, larvae and vectors in the rainy period; however, the positive breeding sites persist in the drought period, a fact that is favored by the mosquito's facility to adapt to the human environment, through natural and/or artificial reservoirs³¹31. Souza SS, Silva IG, Silva HHG. Associação entre incidência de dengue, pluviosidade e densidade larvária de Aedes aegypti , no Estado de Goiás. Rev Soc Bras Med Trop 2010; 43(2): 152-5. ^{, 34}34. Maciel-de-Freitas R, Peres RC, Souza-Santos R, Lourenço-de-Oliveira R. Occurrence, productivity and spatial distribution of key-premises in two dengue-endemic areas of Rio de Janeiro and their role in adult Aedes aegypti spatial infestation pattern. Trop Med Int Health 2008; 13(12): 1488-94. ^{, 40}40. Monteiro ESC, Coelho ME, da Cunha IS, Cavalcante MAS, Carvalho FAA. Aspectos epidemiológicos e vetoriais da dengue na cidade de Teresina, Piauí – Brasil, 2002 a 2006. Epidemiol Serv Saúde 2009; 18(4): 365-74. ^{, 41}41. Codeço CT, Honório NA, Ríos-Velásquez CM, Santos Mda C, Mattos IV, Luz SB, et al. Seasonal dynamics of Aedes aegypti (Diptera: Culicidae) in the northernmost state of Brazil: a likely port-of-entry for dengue virus 4. Mem Inst Oswaldo Cruz 2009 Jul; 104(4): 614-20..

Rainfall and temperature

A study carried out between March 2003 and February 2005 in three districts of high incidence of dengue in the city of Uberlândia, State of Minas Gerais, Southeastern Brazil, showed that temperature and rainfall influenced significantly the increase in the number of breeding sites and the Ae. Aegypti population dynamics . In the rainy period, 86.5% of the exposed traps became positive and only 13.5% in the dry period. When Costa et al.²⁹29. Zeidler JD, Acosta PO, Barrêto PP, Cordeiro Jda D. Dengue virus in Aedes aegypti larvae and infestation dynamics in Roraima, Brazil. Rev Saude Publica 2008; 42(6): 986-91.analyzed colder and drier periods of the year (less favorable conditions to the development of the mosquito), they observed a sharp reduction in the adult population of the vector but, although in a lower proportion, the mosquito was also present in the colder and drier months of the year. This fact has also been described by Dos Reis et al.⁴²42. Dos Reis IC, Honório NA, Codeço CT, Magalhães Mde A, Lourenço-de-Oliveira R, Barcellos C. Relevance of differentiating between residential and non-residential premises for surveillance and control of Aedes aegypti in Rio de Janeiro, Brazil. Acta Trop 2010; 114(1): 37-43., who used oviposition traps in 3 districts of the city of Rio de Janeiro, in the summer (January to March) and in the winter (June to September) of 2007; although the captures did not differ, a higher number of eggs and female adults was verified during the summer.

Dibo et al.⁴³43. Dibo MR, Chierotti AP, Ferrari MS, Mendonça AL, Chiaravalloti Neto F. Study of the relationship between Aedes (Stego­myia) aegypti egg and adult densities, dengue fever and climate in Mirassol, state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2008; 103(6): 554-60., by means of weekly collections of eggs and larvae in the city of Mirassol, state of São Paulo, Southeastern region of Brazil, from November 2004 to November 2005, confirmed the results that have already been described here about Ae. aegypti proliferation, which shows that the number of eggs, larvae and mosquitoes is larger in periods of higher temperatures and rainfall indexes²⁵25. Forattini OP, Kakitani I, dos Santos RLC, Kobayashi KM, Ueno HM, Fernandez Z. Comportamento de Aedes albopictus e Ae. scapularis adultos (Diptera: Culicidae) no sudeste do Brasil. Rev Saúde Pública 2000; 34(5): 461-7. ^{, 26}26. Pinheiro VC, Tadei WP. Frequency, diversity, and productivity study on the Aedes aegypti most preferred containers in the city of Manaus, Amazonas, Brazil. Rev Inst Med Trop Sao Paulo 2002; 44(5): 245-50. ^{, 37}37. Honório NA, Cabello PH, Codeço CT, Lourenço-de-Oliveira R. Preliminary data on the performance of Aedes aegypti and Aedes albopictus immatures developing in water-filled tires in Rio de Janeiro. Mem Inst Oswaldo Cruz 2006; 101(2): 225-8. ^{, 44}44. da Costa-Ribeiro MC, Lourenço-de-Oliveira R, Failloux AB. Geographic and temporal genetic patterns of Aedes aegypti populations in Rio de Janeiro, Brazil. Trop Med Int Health 2006; 11(8): 1276-85..

Monteiro el al.⁴⁰analyzed the epidemiological indicators of dengue in the city of Teresina, state of Piauí, from 2002 to 2006. The authors found a positive correlation between the incidence of dengue, rainfall and temperature, particularly in the first semester of each year, the period with the highest rainfall index and building infestation, mainly in the months of March to May 2002-2003. Such findings corroborate the study conducted by Barbosa and Lourenço³²32. Barbosa GL, Lourenço RW. Análise da distribuição espaço-temporal de dengue e da infestação larvária no município de Tupã, Estado de São Paulo. Rev Soc Bras Med Trop 2010; 43(2): 145-51.in the interior of the State of São Paulo, in the city of Tupã, from January 2004 to December 2007. Larger infestations were noticed in the first quarter of each year, as well as a decrease in the epidemic in June, and an increase in the number of positive reservoirs in the hottest and most humid months of the year (January to April).

In the city of Rio de Janeiro, between 1986 and 2003, it was observed that the largest risk factors for dengue epidemics were: minimum average temperature above 22°C, and hotter and drier summers. The most relevant temperature was that of the first quarter of the analyzed period. It was found that, in the years in which the epidemics occurred, the temperatures were significantly higher when compared to those of the other years. There was no important association between the incidence of the disease and rainfall. The epidemics were more frequent in the years in which the rainfall volume was below 200 mm/month³⁶36. Câmara FP, Gomes AF, Santos GT, Câmara DC. Clima e epidemias de dengue no Estado do Rio de Janeiro. Rev Soc Bras Med Trop 2009; 42(2): 137-40..

Câmara et al.³⁰30. Câmara FP, Theophilo RL, dos Santos GT, Pereira SR, Câmara DC, de Matos RR. Estudo retrospectivo (histórico) da dengue no Brasil: características regionais e dinâmicas. Rev Soc Bras Med Trop 2007; 40(2): 192-6.conducted a time-series study of dengue between 1986 and 2003 in the five regions of Brazil. This study showed that the Northeast and Southeast regions corresponded to approximately 86% of the disease notifications, while the Central-West (7.6%), North (5.7%) and South (1.2%) regions presented a lower number of registers. In 2003, the Northeast and Southeast regions had 70.5% of the Brazilian population, that is, even taking each region's population into account, the disease was more incident in those two regions. In the Southeast, Central-West and South regions, more than half of the cases occurred in the first quarter, while in the Northeast region, it occurred in the second quarter of the year.

However, the epidemiological data of 2008 and 2010 show a change in the distribution pattern of dengue in the country. In 2010, more than one million probable cases of the disease were registered due to the re-circulation of DENV-1, and 63% of the cases occurred in the Central-West and Southeast regions, mainly in cities of the States of Rio de Janeiro, Mato Grosso and Mato Grosso do Sul⁴⁵45. Siqueira JrJB, Vinhal LC, Said RFC, Hoffmann JL, Martins J, Barbiratto SB et al. Dengue no Brasil: tendências e mudanças na epidemiologia, com ênfase nas epidemias de 2008 e 2010. In: Saúde Brasil 2010: uma análise da situação de saúde e de evidências selecionadas de impacto de ações de vigilância em saúde . Brasília: Ministério da Saúde; 2011. pp. 159-171..

The notifications peaks analyzed by the authors³⁰30. Câmara FP, Theophilo RL, dos Santos GT, Pereira SR, Câmara DC, de Matos RR. Estudo retrospectivo (histórico) da dengue no Brasil: características regionais e dinâmicas. Rev Soc Bras Med Trop 2007; 40(2): 192-6.are in agreement with the studies analyzed here. In short, they are concentrated particularly on the first half of each year, a period that is considered the hottest and most humid of the year. In the months in which the temperature decreases, in the second half of the year, it was found that the incidence declined, which shows that the dynamics of the vector and of the disease depends on seasonal variation.

Temperature and relative air humidity

The analysis of an entomological survey that was carried out during 82 weeks, from September 2006 to March 2008, and used ovitrap and mosquiTRAP, showed an important association between the number of positive eggs and incidence of dengue, mainly in the dry period (low rainfall level). The authors³⁵35. Honório NA, Codeço CT, Alves FC, Magalhães MA, Lourenço-De-Oliveira R. Temporal distribution of Aedes aegypti in different districts of Rio de Janeiro, Brazil, measured by two types of traps. J Med Entomol 2009; 46(5): 1001-14.suggest that the monthly average temperature above 22-24° C is strongly associated with Ae. Aegypti abundance and, consequently, with a higher risk of dengue transmission.

Favier et al.³⁹39. Favier C, Degallier N, Vilarinhos PT, de Carvalho MS, Yoshizawa MA, Knox MB. Effects of climate and different management strategies on Aedes aegypti breeding sites: a longitudinal survey in Brasília (DF, Brazil). Trop Med Int Health 2006; 11(7): 1104-18.argued that the number of potential breeding sites follows the rain pattern, but the values are not annulled in the drought period. The mean number of pupae per positive reservoir is intimately associated with the average temperature. It was considered that the variable relative air humidity also favored the number of positive reservoirs in Vila Planalto, Brasília. Similar results in relation to the city of São Sebastião, state of São Paulo⁹9. Ribeiro AF, Marques GR, Voltolini JC, Condino ML. Associação entre incidência de dengue e variáveis climáticas. Rev Saúde Pública 2006; 40(4): 671-6., indicated that the highest values of temperature and relative air humidity were registered from November to April, and it was during these months that the highest indexes of Ae. Aegypti larval density were observed.

A study conducted in the District of Galeão, Ilha do Governador, RJ, between June 1992 and July 1994, revealed that probably only the temperature extremes exercised a differentiated effect on the larvae population. In the following months, or right after the observation of higher registers of relative air humidity, the highest means of the number of positive breeding sites were noted, as well as negative correlations concerning the mean atmospheric pressure⁴⁶46. Souza-Santos R. Fatores associados à ocorrência de formas imaturas de Aedes aegypti na Ilha do Governador, Rio de Janeiro, Brasil. Rev Soc Bras Med Trop 1999; 32(4): 373-82.. Average temperatures between 17 and 23° C were reported as the most favorable for larval development²²22. Gomes Ade C, Forattini OP, Kakitani I, Marques GR, Marques CC, Marucci D et al. Microhabitats de Aedes albopictus (Skuse) na região do Vale do Paraíba, Estado de São Paulo, Brasil. Rev Saude Publica 1992; 26(2): 108-18..

The data described above are corroborated by entomological laboratory studies. The embryonic development of the Ae. Aegypti mosquito was analyzed under the influence of temperature variation and it was observed that the viability of eggs between 16-31°C was higher than 80%; between 22-28°C, it was higher than 90%. Farnesi et al.⁴⁷47. Farnesi LC, Martins AJ, Valle D, Rezende GL. Embryonic development of Aedes aegypti (Diptera: Culicidae): influence of different constant temperatures. Mem Inst Oswaldo Cruz 2009; 104(1): 124-6.highlight that these temperature ranges favor the Ae. Aegypti presence in the tropical and subtropical regions of the world.

Miyazaki et al.⁴⁸48. Miyazaki RD, Ribeiro AL, Pignatti MG, Campelo JHJr, Pignati M. Monitoring of Aedes aegypti mosquitoes (Linnaeus, 1762) (Diptera: Culicidae) by means of ovitraps at the Universidade Federal de Mato Grosso Campus, Cuiabá, State of Mato Grosso. Rev Soc Bras Med Trop 2009; 42(4): 392-97.carried out a monitoring study that employed ovitraps in the city of Cuiabá, state of Mato Grosso, between August 2004 and August 2005. Cuiabá is one of the hottest capital cities of Brazil, with maximum averages around 31º C. This study showed a significant correlation with maximum, average and minimum temperature. However, the authors⁴⁸48. Miyazaki RD, Ribeiro AL, Pignatti MG, Campelo JHJr, Pignati M. Monitoring of Aedes aegypti mosquitoes (Linnaeus, 1762) (Diptera: Culicidae) by means of ovitraps at the Universidade Federal de Mato Grosso Campus, Cuiabá, State of Mato Grosso. Rev Soc Bras Med Trop 2009; 42(4): 392-97.considered that rainfall was the only determinant factor for infestation level. The frequency of egg collection showed an increase in the months of October and December, totaling 49% and 36.8%, respectively. A larger presence of females was observed in the months of July and August and there was no association between number of eggs and relative air humidity. The number of collections did not follow one single distribution pattern over the period. It could occur during the whole year, as it has been shown in other studies²⁸28. Costa FS, Silva JJ, Souza CM, Mendes J. Dinâmica populacional de Aedes aegypti (L) em área urbana de alta incidência de dengue. Rev Soc Bras Med Trop 2008; 41(3): 309-12. ^{, 43}43. Dibo MR, Chierotti AP, Ferrari MS, Mendonça AL, Chiaravalloti Neto F. Study of the relationship between Aedes (Stego­myia) aegypti egg and adult densities, dengue fever and climate in Mirassol, state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2008; 103(6): 554-60. ^{, 49}49. Marques GR, Gomes Ade C. Comportamento antropofílico de Aedes albopictus (Skuse) (Diptera: Culicidae) na região do Vale do Paraíba, Sudeste do Brasil. Rev Saúde Pública 1997; 31(2): 125-30..

Lag

In spite of the fact that meteorological variations are an important predictor, it is known that in the majority of the situations there is a time lag, that is, a lag in the association between meteorological variables and the occurrence of dengue or the emergence of new larvae/mosquitoes in the same month.

Ribeiro et al.⁹9. Ribeiro AF, Marques GR, Voltolini JC, Condino ML. Associação entre incidência de dengue e variáveis climáticas. Rev Saúde Pública 2006; 40(4): 671-6.analyzed the time lag of the association between the number of cases of dengue and abiotic factors (rain and temperature) in the city of São Sebastião, state of São Paulo, from 2001 to 2002. The authors identified that the lag revealed a significant association in the second, third and fourth months of observation, that is, the rain and temperature of a given month contributed to explain the number of cases of dengue two to four months later.

The analysis of the incidence of dengue in the state of Paraíba through distributed lag models found that the coefficients decrease up to the fourth month and increase again in the fifth month. The beginning of the annual growth curves occurs five months in advance, which corresponds to a five-month lag. Therefore, a different curve of dengue incidence occurred in each year, and the peaks oscillate between the months of March and May. For this reason, Souza^{et al. 27}27. Souza IC, Vianna RP, Moraes RM. Modelagem da incidência do dengue na Paraíba, Brasil, por modelos de defasagem distribuída. Cad Saúde Pública 2007; 23(11): 2623-30.stated that the five-month lag corresponds to the duration of the period that is necessary for a change to occur in the trend of the annual curve of dengue incidence, from the beginning of the summer onwards.

Oliveira et al.⁵⁰50. Oliveira CL, Bier VA, Maier CR, Rorato GM, Frost KF; Barbosa MA et al. Incidência da dengue relacionada às condições climáticas no município de Toledo – PR. Arq Ciências Saúde UNIPAR 2007; 11(3): 211-6., in a study carried out in the city of Toledo, state of Paraná, from November 2001 to July 2002, observed a 20.5% correlation regarding the influence of rainfall on the number of confirmed cases in the following month. This correlation practically does not exist concerning two or three months after the rain period.

Final remarks

The research showed that meteorological factors such as temperature, relative air humidity and rainfall, mentioned in the studies analyzed here, influenced the vector dynamics, as well as the peaks of the dengue epidemics in Brazil, independently of the climate zone. The occurrence of the disease is associated with increased rainfall indexes and with temperature variations, mainly in the first semester of each year. This is the period of highest temperature and rainfall levels in the largest part of Brazil, which contributes to increase the number of breeding sites and, consequently, the number of cases of dengue.

Even though this disease is typically seasonal, cases of dengue are registered both in the rainy and dry periods, as the reduction in the vector density of adults in the cold and dry months is not enough to cease the disease transmission. There are, however, countless difficulties in establishing a “key” seasonal pattern of the incidence of the disease and of the meteorological variables, due to the fact that the vector's blood-feeding pattern occurs predominantly during the whole year, with different intensities.

Brazil's large territorial dimension must be taken into account, as well as its border with neighboring countries, the diversity of biomes, lack of urban infrastructure, and favorable meteorological and environmental characteristics during almost the whole year, which facilitate the maintenance of the disease. In the majority of the studies analyzed here, the highest vector density coincides with the rainy period, suggesting that rainfall is the most important abiotic factor for the increase in the vector population. In this sense, it should be highlighted that the rain cycle in Brazil has peculiar characteristics, according to the different climate zones in the distinct geographical regions. There is no homogeneous distribution of rainfall levels in the national territory.

Other relevant aspects are the genetic complexity of the vector and the circulation of different serotypes, which are likely to influence the dengue distribution, both in the dry and rainy periods, and the vector's capacity to adapt to the human environment through breeding sites. Therefore, the vector does not depend exclusively on abiotic factors. It survives in low density during the months that are less favorable in climatic terms, which shows the relevance of maintaining the actions of vector surveillance and control during the entire year.

As this is a scientific literature review, the study is potentially conditioned to the biases of the reviewed studies, that is, it depends on the findings contained in the publications. Another bias concerns the distribution of the studies, which was concentrated particularly on some States. Based on this systematic review, it was found that all the Brazilian climates were represented if the areas of study are considered. However, the best represented climate was the Central Brazil Tropical Climate, which coincides with the most populated area, and also with the most endemic area of the country.

It is concluded that dengue is strongly related to meteorological variables. The seasonal variation of temperature and rainfall influenced the vector dynamics and the incidence of the disease in the entire country, independently of the climate zone.

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