ABSTRACT

OBJECTIVE

To describe the epidemiology of dengue in a medium-sized city in the state of São Paulo.

METHODS

Data, such as circulating serotypes, severe cases and deaths, age group, sex, among others, were obtained on reported and confirmed dengue cases in Araraquara, state of São Paulo, between 1991 and 2015. Climatic and infestation data were also analyzed. These variables were evaluated descriptively, using statistical measures such as frequencies, averages, minimum and maximum. Dengue incidence rates were calculated according to month, year, age and sex, and time series of dengue cases, infestation, and climatic variables.

RESULTS

Approximately 16,500 cases of dengue fever were reported between 1991 and 2015. The highest number of reports was recorded in 2015 (7,811 cases). In general, the age group with the highest number of reports is between 20 and 59 years old. The highest incidences, generally between March and May, occurred after the increase in rainfall and infestation in January.

CONCLUSIONS

Increased levels of infestation due to rainfall are reflected in incidence rates of the disease. It is fundamental to know the epidemiology of dengue in medium-sized cities. Such information can be extended to diseases such as Zika and Chikungunya, which are transmitted by the same vector and were reported in the city. The intensification of surveillance efforts in periods before epidemics could be a strategy to be considered to control the viral spread.

Dengue, epidemiology; Disease Outbreaks; Risk Factors; Communicable Diseases; Epidemiological Surveillance

INTRODUCTION

Dengue is a viral disease that is a major public health problem. It entails 20 thousand deaths and 500 thousand hospitalizations annually. In addition, 390 million people are infected each year, but only 96 million cases are symptomatic⁵5. 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... ^,2020. Idrees S, Ashfaq UA. A brief review on dengue molecular virology, diagnosis, treatment and prevalence in Pakistan. Genet Vaccines Ther. 2012;10(1):6. https://doi.org/10.1186/1479-0556-10-6
https://doi.org/10.1186/1479-0556-10-6... . The disease is caused by one of the four serotypes of the dengue virus (DENV 1-4), which are transmitted by mosquitoes of the genus Aedes³⁹39. World Heatlh Organization. Dengue: guidelines for diagnosis, treatment, prevention and control. Geneva: WHO; 2009.. Aedes aegypti is the most important vector of dengue, zika, and chikungunya in Brazil³⁴34. Souza LJ. dengue, zika e chikungunya: diagnóstico, tratamento e prevenção. Rio de Janeiro: Rubio; 2016.. The genus Flavivirus, Flaviviridae family, circulates in Asia, Africa, the Americas and more recently in Europe¹³13. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, et al. Dengue: a continuing global threat. Nat Rev Microbiol. 2010;8(12 Suppl):S7-16. https://doi.org/10.1038/nrmicro2460
https://doi.org/10.1038/nrmicro2460... .

The spatial distribution of these vectors strongly affects the epidemiology of the disease. In addition, the life cycle of Ae. aegypti is almost completely dependent on the environments created by humans and varies according to changes and climatic fluctuations¹⁴14. Higa Y. Dengue vectors and their spatial distribution. Trop Med Health. 2011;39(4 Suppl):17-27. https://doi.org/10.2149/tmh.2011-S04
https://doi.org/10.2149/tmh.2011-S04... . The increase in temperature, variations in rainfall and relative air humidity favor the number of breeding sites available and the development of the vector³⁵35. Viana DV, Ignotti E. A ocorrência da dengue e variações meteorológicas no Brasil: revisão sistemática. Rev Bras Epidemiol. 2013;16(2):240-56. https://doi.org/10.1590/S1415-790X2013000200002
https://doi.org/10.1590/S1415-790X201300... .

Dengue is a global concern, and the current trends are: rapidly expanding the geographical distribution of the vector and spread of the virus. In addition, the continuous circulation of the four serotypes is associated with the magnitude of the epidemics and the increase of severe manifestations and deaths due to infection. Reports of dengue fever in Brazil have increased dramatically since the 1980s. Rapid and unplanned urbanization poor living conditions, and inefficiency of surveillance and vector control are some of the factors related to the dispersion of DENV³3. Bäck AT, Lundkvist A. Dengue viruses - an overview. Infect Ecol Epidemiol. 2013;3(1):19839. https://dx.doi.org/10.3402/iee.v3i0.19839
https://dx.doi.org/10.3402/iee.v3i0.1983... ^,1111. Ferreira GLC. Global dengue epidemiology trends. Rev Inst Med Trop Sao Paulo. 2012;54 Supl 18:S5-6. https://doi.org/10.1590/S0036-46652012000700003
https://doi.org/10.1590/S0036-4665201200... .

In addition to dengue, chikungunya (CHIKV) and zika (ZIKV) are equally worrying arboviruses in expansion in Brazil. The first belongs to the Togaviridae family, and was reported in the country in September 2014. It affected 2,772 people in the North and Midwest regions that same year. ZIKV is also a Flavivirus that dispersed throughout the country and were first reported in Bahia, in April 2015³⁴34. Souza LJ. dengue, zika e chikungunya: diagnóstico, tratamento e prevenção. Rio de Janeiro: Rubio; 2016..

The increase in the number and severity of dengue cases in Brazil and worldwide demands investigations to identify patterns of transmission in cities with similar attributes. Knowing the epidemiological and clinical aspects of the disease in endemic areas is essential for the implementation of interventions to modify transmission patterns. The study of dengue fever and its relationship with vectors and climatic variables can also identify areas at risk for ZIKV and CHIKV infections. Ae. aegypti is known to be also a vector of these viruses, which makes it possible to map out common surveillance and control strategies¹1. Augusto LGS, Gurgel AM, Costa AM, Diderichsen F, Lacaz FA, Parra-Henao G, et al. Aedes aegypti control in Brazil. Lancet. 2016;387(10023):1052-53. https://dx.doi.org/10.1016/S0140-6736(16)00626-7
https://dx.doi.org/10.1016/S0140-6736(16... ^,1010. Faria NR, Azevedo RSS, Kraemer MUG, Souza R, Cunha MS, Hill SC, et al. Zika virus in the Americas: early epidemiological and genetic findings. Science. 2016;352(6283):345-9. https://doi.org/10.1126/science.aaf5036
https://doi.org/10.1126/science.aaf5036... .

The objective of this study was to describe the epidemiology of dengue in a medium-sized city in the state of São Paulo.

METHODS

Located in the southeastern region of Brazil, the state of São Paulo concentrates 22% of the Brazilian population. It is the most densely populated state in the country and the third most populous political unit in South America¹²12. Governo do Estado de São Paulo. Uma potência chamada São Paulo. São Paulo; c2016 [cited 2016 Sep 15]. Available from: http://www.saopaulo.sp.gov.br/conhecasp/principal_conheca
http://www.saopaulo.sp.gov.br/conhecasp/... . São Paulo is divided into 645 municipalities and has the second highest Human Development Index (HDI) in Brazil.

Araraquara (21º47’40” south latitude, 48º10’32” west longitude) stands out, regionally and nationally, in terms of quality of life (HDI = 0.815). The city has an estimated population of 226,508 inhabitants, a territorial area of 109.88 km² and 206.68 inhabitants/km².¹⁹19. Instituto Brasileiro de Geografia e Estatística. Estimativas populacionais para os municípios e para as Unidades da Federação brasileiros em 01.07.2015. Rio de Janeiro: IBGE; s.d. [cited 2016 Sep 15]. Available from: http://www.ibge.gov.br/home/estatistica/populacao/estimativa2015/default.shtm
http://www.ibge.gov.br/home/estatistica/...

It is located in the center of São Paulo, 270 km from the capital. It is one of the most industrialized cities in the state. Its economy is focused on manufacturing (food, aeronautics, chemical-pharmaceutical and civil construction), agribusiness (sugar, ethanol and orange juice) and commerce and services, as well as on education (several public and private universities) (Figure 1).

A descriptive and retrospective epidemiological study was carried out to establish a profile of the dengue occurrence in Araraquara. Health-related aspects of human populations, such as age, sex, socioeconomic level, geographical location, among other variables²⁹29. Porta M. A dictionary of epidemiology. 5.ed. New York: Oxford University Press; 2008. were considered.

Dengue reports were recovered from (i) Epidemiological Surveillance Center website (CVE)⁸8. Centro de Vigilância Epidemiológica “Prof. Alexandre Vranjac”. Dados Estatísticos. São Paulo: CVE; 2015 [cited 2016 Sep 15]. Available from: http://portal.saude.sp.gov.br/cve-centro-de-vigilancia-epidemiologica-prof.-alexandre-vranjac/areas-de-vigilancia/doencas-de-transmissao-por-vetores-e-zoonoses/agravos/dengue/dados-estatisticos
http://portal.saude.sp.gov.br/cve-centro... , for the cases occurred between 1991 and 2007; and (ii) with the Special Health Service of Araraquara (SESA), through the Information System on Diseases of Compulsory Declaration (SINAN)²⁴24. Ministério da Saúde (BR). Guia de vigilância epidemiológica. 6. ed. Brasília (DF); 2005 [cited 2016 Sep 15]. (Série A. Normas e Manuais Técnicos). Available from: http://bvsms.saude.gov.br/bvs/publicacoes/Guia_Vig_Epid_novo2.pdf
http://bvsms.saude.gov.br/bvs/publicacoe... , for cases occurring between 2008 and 2015. Demographic and socioeconomic information provided by the Brazilian Institute of Geography and Statistics (IBGE), as well as the geographical databases of Araraquara, São Paulo, Brazil and South America (Universal Transverse Mercator [UTM], zone 22S, WGS 1984)¹⁸18. Instituto Brasileiro de Geografia e Estatística. Censo demográfico 2010. Rio de Janeiro: IBGE; s.d. [cited 2013 Oct 10]. Available from: http://www.ibge.gov.br/home/estatistica/populacao/censo2010/default.shtm
http://www.ibge.gov.br/home/estatistica/... .

The climatic information (average rainfall, humidity, and temperature) was collected monthly and yearly on the website of Centro Integrado de Informações Agrometeorológicas (CIIAGRO)^aaCentro Integrado de Informações Aagrometeorológicas. São Paulo: CIIAGRO; s.d. [cited 2016 Sep 15]. Available from: http://www.ciiagro.sp.gov.br , Companhia Ambiental do Estado de São Paulo (CETESB)^bbCompanhia Ambiental de Estado de São Paulo. Sistema de Informações da Qualidade do Ar - QUALAR. São Paulo: CETESB; s.d. [cited 2015 Sep 15]. Available from: http://ar.cetesb.sp.gov.br/qualar/ and Departamento Autônomo de Água e Esgotos de Araraquara (DAAE)^cc São Paulo (Estado), Secretaria de Saneamento e Recursos Hídricos, Departamento de Águas e Energia Elétrica. Hidrologia: banco de dados hidrológicos. São Paulo: DAEE; s.d. [cited 2016 Sep 15]. Available from: http://www.hidrologia.daee.sp.gov.br .

The positivity of the strategic points (StP) obtained from the Superintendência de Controle de Endemias (Sucen SR-06) was used as a measure of larval infestation. The StP are real estate with greater importance in the generation and active and passive dispersion of Ae. aegypti. Deposits of tires junkyard, automobile dismantling workshops, rubber shops, factories, cemeteries, transporters, road and rail stations, ports and airports are considered important strategic points. The positivity of these properties is calculated by the number of positive properties for Ae. aegypti (×100) divided by the number of properties that were assessed. These measures are carried out monthly^ddSecretaria de Estado de Saúde de São Paulo, Superintendência de Controle de Endemias. São Paulo: SUCEN; 2016 [cited 2017 Oct 26]. Available from: http://www.saude.sp.gov.br/resources/sucen/homepage/downloads/arquivos-dengue/norte.pdf .

Time series were constructed from the data referring to the occurrence of dengue in Araraquara between 1991 and 2015. In the first series, the first imported case up to the autochthonous cases of 2015 were included in the analysis, as well as the circulating serotypes, severe cases, and deaths due to infection. We considered all dengue cases confirmed by laboratory or clinical-epidemiological criteria, as recommended by the Ministry of Health²⁴24. Ministério da Saúde (BR). Guia de vigilância epidemiológica. 6. ed. Brasília (DF); 2005 [cited 2016 Sep 15]. (Série A. Normas e Manuais Técnicos). Available from: http://bvsms.saude.gov.br/bvs/publicacoes/Guia_Vig_Epid_novo2.pdf
http://bvsms.saude.gov.br/bvs/publicacoe... .

Information from 1991 to 2007 was presented to provide a historical parameter of dengue transmission in the city. However, the secondary data were limited and could not be used in the descriptive analysis for this period.

Dengue cases reported between 2008 and 2015, climatic variables, and positivity of monthly StP were associated to generate a second time series. Cases of dengue were presented as percentages, dividing the number of cases of each month by the total number of cases of the respective year (×100). This procedure was used to standardize curves of cases per dengue-year, since there could be distortions if absolute numbers were used. The relationship between the occurrence of dengue, the entomological indexes, and the climatic variables could be visualized comparing the formats of the monthly curves.

Cases were organized by dengue-year, a criterion commonly used in epidemiological studies of dengue²⁵25. Mondini A, Chiaravalloti Neto F, Gallo-y-Sanches M, Lopes JCC. Análise espacial da transmissão de cidade de porte médio do interior paulista. Rev Saude Publica. 2005;39(3):444-51. https://doi.org/10.1590/S0034-89102005000300016
https://doi.org/10.1590/S0034-8910200500... . In this approach, data are analyzed considering cases reported between September of a year to August of the following year to evidence the seasonality of the disease.

Data were organized based on the date of the onset of the disease and analyzed according to gender, age, classification and evolution of the case (cure, death due to dengue, death due to other causes). We used World Health Organization revised classification of dengue which was adopted in 2014: dengue without warning signs, dengue with signs of alarm and severe dengue)³⁹39. World Heatlh Organization. Dengue: guidelines for diagnosis, treatment, prevention and control. Geneva: WHO; 2009.. Gross incidence rates per month and year were calculated for the entire period.

The incidence adjusted by age and sex was estimated for each year, applying the direct method²¹21. Jekel JF, Katz DL, Elmore JG, Wild DMG. Epidemiology, biostatistics, and preventive medicine. 3.ed. Philadelphia: Saunders; 2007.. This is the most common strategy to remove the effect of bias due to different age structures in different populations or in the same population at different periods. This adjustment was performed by multiplying incidence rates by age group with specific weights for the same range for each year. The weights within each age group were calculated with the proportion of São Paulo state population, based on 2010 demographic census and estimates of population per year. The adjustment of cases by age provided age-adjusted incidence rates of dengue for each year of the period.

RESULTS

The first confirmed dengue case in Araraquara was imported and occurred in 1991 (Figure 2). Between 1991 and 2015, 16,431 cases were reported, and the first outbreak occurred in 2008. Severe cases and deaths were reported as of 2010. Information on circulating serotype(s) was not available until 2007. The detection of DENV-3 serotype in 2008, DENV-1 in 2010 and DENV-1, 2 and 3 in 2015, was performed through viral isolation of a small percentage of patients.

We recovered 15,729 dengue cases, distributed per dengue-year, between September 2007 and August 2015. The first dengue outbreak in 2008 had an incidence of 639 cases per 100,000 inhabitants. The most severe outbreak in the time series had an incidence of 3,448 cases per 100,000 inhabitants and occurred in 2015. The periods between March and May presented the highest incidences. However, an increase in dengue reports was noticed as of January. Autochthonous cases in all months of the year started to occur in 2008 (Figure 3, A and B).

The most affected age group in the eight-year period was from 20 to 39 years (Figure 3, C). The age-adjusted incidence was slightly higher for females (Figure 3, D). However, a higher difference in this percentage was noticed for 2015.

The increase of precipitation and humidity curves were followed by the positivity of strategic points (Figure 4). Precipitation and humidity growth were key factors for the increase of Ae. aegypti infestation. In addition, case curves increased one or two months after the peaks of rainfall and infestation. There is an apparent relationship between the increase of temperature and infestation growth and dengue cases, although this relation seems discrete.

DISCUSSION

There was an increase in the number of months with dengue cases over the years, especially the ones considered interepidemic. Thus, we could describe the process of dengue endemization in the city. This process refers to the occurrence of dengue cases in every month of the year, with no introduction of serotypes. According to Mondini et al.²⁵25. Mondini A, Chiaravalloti Neto F, Gallo-y-Sanches M, Lopes JCC. Análise espacial da transmissão de cidade de porte médio do interior paulista. Rev Saude Publica. 2005;39(3):444-51. https://doi.org/10.1590/S0034-89102005000300016
https://doi.org/10.1590/S0034-8910200500... , endemization allows a continuous viral transmission, since the occurrence of dengue in the previous summer guarantees the occurrence of transmission in the following season.

The first major dengue outbreak occurred in São Paulo in 1990, resulting in viral circulation in a large portion of the state²2. Azevedo TS, Piovezan R, Von Zuben CJ, André IRN, Almeida D. Perfil epidemiológico da dengue no município de Rio Claro no período de 1996 a 2010. Hygeia. 2011 [cited 2016 Sep 15];7(12):19-30. Available from: http://www.seer.ufu.br/index.php/hygeia/article/view/16980
http://www.seer.ufu.br/index.php/hygeia/... . Although Araraquara was infested by Ae. aegypti since 1986, the first dengue epidemic in the city (2008) occurred late when compared to proximate cities. Ribeirão Preto¹⁵15. Hino P, Santos CC, Santos MO, Cunha TN, Santos CB. Evolução temporal da dengue no município de Ribeirão Preto, São Paulo, 1994 a 2003. Cienc Saude Coletiva. 2010;15(1):233-8. https://doi.org/10.1590/S1413-81232010000100028
https://doi.org/10.1590/S1413-8123201000... and São José do Rio Preto, located respectively 93 km and 170 km away from Araraquara, experienced the first outbreaks in 1990^eeChiaravalloti-Neto F. Epidemiologia da dengue nas regiões de São José do Rio Preto e Araçatuba, São Paulo, 1990 a 1996 [these]. São Paulo: Faculdade de Saúde Pública da Universidade de São Paulo; 1999..

The growth of dengue cases in Araraquara in 2008 may be related to the introduction of DENV-3 in 2007. Differently from what occurred in Brazil and the state of São Paulo, where DENV-3 circulated since 2001²⁶26. Nogueira RMR, Schatzmayr HG, Filippis AMB, Santos FB, Cunha RV, Coelho JO, et al. Dengue virus type 3, Brazil, 2002. Emerg Infec Dis. 2005;11(9):1376-81. https://doi.org/10.3201/eid1109.041043
https://doi.org/10.3201/eid1109.041043... ^,3737. Villabona-Arenas CJ, Mondini A, Bosch I, Schimidt D, Calzavara-Silva CE, Zanotto PMA, et al. Dengue virus type 3 adaptive changes during epidemics in São Jose de Rio Preto, Brazil, 2006-2007. PloS One. 2013;8(5):e63496. https://doi.org/10.1371/journal.pone.0063496
https://doi.org/10.1371/journal.pone.006... , this late introduction might have favored this outbreak, due to the susceptibility of the population to this serotype. The first severe cases occurred in 2010, when DENV-1 and 2 were circulating. The circulation of both serotypes influenced the next outbreak (2011).

The major epidemics in Araraquara were followed by outbreaks in neighboring municipalities such as Matão, Rincão, Motuca and Américo Brasiliense⁸8. Centro de Vigilância Epidemiológica “Prof. Alexandre Vranjac”. Dados Estatísticos. São Paulo: CVE; 2015 [cited 2016 Sep 15]. Available from: http://portal.saude.sp.gov.br/cve-centro-de-vigilancia-epidemiologica-prof.-alexandre-vranjac/areas-de-vigilancia/doencas-de-transmissao-por-vetores-e-zoonoses/agravos/dengue/dados-estatisticos
http://portal.saude.sp.gov.br/cve-centro... . This trend reinforces its role as a disseminator or receptor of DENV. Araraquara is the most populated city in the micro-region¹⁹19. Instituto Brasileiro de Geografia e Estatística. Estimativas populacionais para os municípios e para as Unidades da Federação brasileiros em 01.07.2015. Rio de Janeiro: IBGE; s.d. [cited 2016 Sep 15]. Available from: http://www.ibge.gov.br/home/estatistica/populacao/estimativa2015/default.shtm
http://www.ibge.gov.br/home/estatistica/... , and stands out economically for its commerce and education resources, causing intense human migration to the city. Roseghini et al.³²32. Roseghini WFF, Mendonça F, Ceccato P, Fernandes K. Dengue epidemics in Middle-South of Brazil: climate contraints and some social aspects. Rev Bras Climatol. 2011 [cited 2016 Sep 15];(9):94-101. Available from: http://revistas.ufpr.br/revistaabclima/article/viewFile/27522/18336
http://revistas.ufpr.br/revistaabclima/a... showed that socioeconomic factors favor the flow of people from smaller to larger cities in search of better health services, or for work and leisure. This migration of the population could play a key role in the occurrence of epidemics. This association is little known and deserves further studies.

Araraquara presented an expressive increase in number and severity of cases and deaths. Paixão et al.²⁷27. Paixão ES, Costa MCN, Rodrigues LC, Rasella D, Cardim LL, Brasileiro AC, et al. Trends and factors associated with dengue mortality and fatality in Brazil. Rev Soc Bras Med Trop. 2015;48(4):399-405. https://doi.org/10.1590/0037-8682-0145-2015
https://doi.org/10.1590/0037-8682-0145-2... demonstrated the risk of death due to dengue increased significantly between 2000 and 2011 in all regions of Brazil. A study in Amazonas indicated that 88% of dengue-confirmed deaths had been identified by health services as severe cases. A more careful attention to signs of dengue could have contributed to reducing disease mortality²⁸28. Pinto RC, Castro DB, Albuquerque BC, Sampaio VS, Passos RA, Costa CF, et al. Mortality predictors in patients with severe dengue in the State of Amazonas, Brazil. PLoS One. 2016;11(8):e0161884. https://doi.org/10.1371/journal.pone.0161884
https://doi.org/10.1371/journal.pone.016... . A recent review indicates that early diagnosis and immediate treatment of severe cases may reduce disease severity and mortality³⁸38. Wilder-Smith A, Byass P. The elusive global burden of dengue. Lancet Infect Dis. 2016;16(6):629-31. https://doi.org/10.1016/S1473-3099(16)00076-1
https://doi.org/10.1016/S1473-3099(16)00... .

We did not investigate severe cases and deaths in particular, but the most affected age group in the period was between 20 and 59 years. This group corresponds to the economically active population, who works or studies during the day. Women presented a small difference in the distribution of cases and were more affected than men. The same patterns for age group and gender was observed in a study carried out in São José do Rio Preto³³33. Scandar SAS, Vieira P, Cardoso Junior RP, Silva RA, Papa M, Sallum MAM. Dengue em São José do Rio Preto, Estado de São Paulo, Brasil, 1990 a 2005: fatores entomológicos, ambientais e socioeconômicos. Bol Epidemiol Paul. 2010 [cited 2016 Sep 15];7(81):4-16. Available from: http://periodicos.ses.sp.bvs.br/pdf/bepa/v7n81/v7n81a01.pdf
http://periodicos.ses.sp.bvs.br/pdf/bepa... . A higher incidence in women from different regions may be related to the fact that they tend to seek more medical care than men. This observation may represent a bias in comparisons of incidence rates⁷7. Cavalcante WD, Vilar MSA, Vilar DA, Soares CS. Características epidemiológicas da dengue na comunidade São Januário II na cidade de Campina Grande - PB. Rev Bras Farm. 2011 [cited 2016 Sep 15];92(4):287-94. Available from: http://www.rbfarma.org.br/files/rbf-2011-92-4-7-287-294.pdf
http://www.rbfarma.org.br/files/rbf-2011... .

Incidence rates in Araraquara presented seasonal trends, increasing after the growth of infestation, which was followed by the elevation of rainfall. The increment in case numbers from March to May have resulted from the rainfall in January and March. This indicates a pattern in which rainfall in one month causes an increase in the number of cases in the subsequent two months. A higher rainfall influenced the availability of oviposition sites³⁵35. Viana DV, Ignotti E. A ocorrência da dengue e variações meteorológicas no Brasil: revisão sistemática. Rev Bras Epidemiol. 2013;16(2):240-56. https://doi.org/10.1590/S1415-790X2013000200002
https://doi.org/10.1590/S1415-790X201300... and caused an increase in infestation that was observed. Several studies found a similar pattern between rainfall and dengue incidences⁹9. Dibo MG, 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. https://doi.org/10.1590/S0074-02762008000600008
https://doi.org/10.1590/S0074-0276200800... ^,2222. Johansson MA, Dominici F, Glass GE. Local and global effects of climate on dengue transmission in Puerto Rico. PLoS Negl Trop Dis. 2009;3(2):e382. https://doi.org/10.1371/journal.pntd.0000382
https://doi.org/10.1371/journal.pntd.000... ^,3030. Ramadona AL, Lazuardi L, Hii YL, Holmner A, Kusnanto H, Rocklov J. Prediction of dengue outbreaks based on disease surveillance and meteorological data. PLoS One. 2016;11(3):e0152688. https://10.1371/journal.pone.0152688
https://10.1371/journal.pone.0152688... . These results may be useful for the development of policies for dengue control and prevention.

The association between temperature and infestation was mild and did not seem to influence incidence rates. In general, summer and winter presented high temperatures, which are adequate for vector proliferation. A study in the city of São Paulo demonstrated that dengue incidence was more affected by temperature²2. Azevedo TS, Piovezan R, Von Zuben CJ, André IRN, Almeida D. Perfil epidemiológico da dengue no município de Rio Claro no período de 1996 a 2010. Hygeia. 2011 [cited 2016 Sep 15];7(12):19-30. Available from: http://www.seer.ufu.br/index.php/hygeia/article/view/16980
http://www.seer.ufu.br/index.php/hygeia/... . The increase in temperature influenced the dynamics of Ae. aegypti and, consequently, the transmission of the dengue virus⁴4. Barbazan P, Guiserix M, Boonyum W, Tuntaprasart W, Pontier D, Gonzalez JP. Modelling the effect of temperature on transmission of dengue. Med Vet Entomol. 2010;24(1):66-73. https://doi.org/10.1111/j.1365-2915.2009.00848.x
https://doi.org/10.1111/j.1365-2915.2009... ^,3131. Richardson K, Hoffmann AA, Johnson P, Ritchie S, Kearney MR. Thermal sensivity of Aedes aegypti from Australia: empirical data and prediction of effects on distribution. J Med Entomol. 2011;48(4):914-923. https://doi.org/10.1603/ME10204
https://doi.org/10.1603/ME10204... .

According to Viana and Ignotti³⁵35. Viana DV, Ignotti E. A ocorrência da dengue e variações meteorológicas no Brasil: revisão sistemática. Rev Bras Epidemiol. 2013;16(2):240-56. https://doi.org/10.1590/S1415-790X2013000200002
https://doi.org/10.1590/S1415-790X201300... , meteorological variables such as temperature, humidity and rainfall influence the vector dynamics and incidences of dengue in Brazil. Rainfall and temperature favor an increase in breeding sites and dengue cases. In dry and low-temperature periods, there is a decrease in the number of vectors, but it is not enough to stop the transmission of the disease, due to the avid hematophagous behavior of the vector which favors virus dispersion. Horta et al.¹⁷17. Horta MA, Bruniera R, Ker F, Catita C, Ferreira AP. Temporal relationship between environmental factors and the occurrence of dengue fever. Int J Environ Health Res. 2014;24(5):471-81. https://doi.org/10.1080/09603123.2013.865713
https://doi.org/10.1080/09603123.2013.86... have shown that models based on climatic variables that consider the interval between rainfall, temperature and dengue can be useful in dengue control programs in tropical countries.

Epidemiological surveillance of dengue is mainly based in monitoring the density of vector infestation, to avoid levels of infestation capable of sustaining transmission and monitoring human cases to detect the early onset of outbreaks³⁴34. Souza LJ. dengue, zika e chikungunya: diagnóstico, tratamento e prevenção. Rio de Janeiro: Rubio; 2016.. In our study, we were able to demonstrate aspects that favor the occurrence of dengue in Araraquara. These aspects could be useful for the development of effective surveillance strategies resulting in adoption of more adequate control measures to reduce or slow the transmission. For effective surveillance, early recognition of local transmission is necessary, followed by rapid and effective vector control and other measures that incorporate the ecological, entomological and virological components¹⁶16. 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... .

In Brazil, the major epidemics caused by these viruses occur due to the widespread infestation of vectors throughout the territory and the susceptibility of the population, which contributes to DENV dissemination¹⁶16. 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... . Another key factor is the delay of the surveillance system in early recognizing transmission and initiating effective control measures in a timely manner. According to Viennet et al.³⁶36. Viennet E, Ritchie SA, Faddy HM, Williams CR, Harley D. Epidemiology of dengue in a high-income country: a case study in Queensland, Australia. Parasit Vectors. 2014;7:379. https://doi.org/10.1186/1756-3305-7-379
https://doi.org/10.1186/1756-3305-7-379... , the delay in reporting cases is a crucial determinant of DENV transmission. They suggest that future research should include analyses of areas with high rates people migration alongside demographic, socioeconomic and entomological factors. As seen in Araraquara, knowledge of DENV epidemiology provided information on the most appropriate moment to start dengue control programs. In addition, these actions could also be guidelines for surveillance and control of zika and chikungunya. Both viruses are transmitted by the same vector and presented autochthonous transmission in the city⁸8. Centro de Vigilância Epidemiológica “Prof. Alexandre Vranjac”. Dados Estatísticos. São Paulo: CVE; 2015 [cited 2016 Sep 15]. Available from: http://portal.saude.sp.gov.br/cve-centro-de-vigilancia-epidemiologica-prof.-alexandre-vranjac/areas-de-vigilancia/doencas-de-transmissao-por-vetores-e-zoonoses/agravos/dengue/dados-estatisticos
http://portal.saude.sp.gov.br/cve-centro... .

This is the first study on dengue epidemiology in Araraquara, and like most descriptive epidemiological studies, presented limitations. These include the lack of information on cases reported prior to 2007; the fact that it was conducted using secondary data, and lack of molecular surveillance with differential diagnosis of circulating serotypes in the city. Despite these limitations, our study showed the importance of knowing the epidemiological aspects of dengue in medium-sized endemic municipalities, between 150 and 250 thousand inhabitants. Actions in these areas can guide actions in other municipalities with similar characteristics.

Kularatne²³23. Kularatne SAM. Dengue fever. BMJ. 2015;351:h4661. https://doi.org/10.1136/bmj.h4661
https://doi.org/10.1136/bmj.h4661... concluded that the key to all prevention programs is surveillance to detect early outbreaks. This study showed that the incidence of dengue begins to increase in the month of January, which coincides with rain peaks. This increase in rainfall is reflected in the incidence rates in the subsequent months. This period may be indicative of when to start disease control measures. It is recommended that surveillance services initiate an active search for cases and areas infested by Ae. aegypti when the rainfall is identified. From there, vector control measures must be intensified in these areas, as well as the dissemination of these measures to the population through media campaigns and other means of communication. It is important to increase attention to the first symptoms of the disease and measures to eliminate water accumulation, avoiding the birth and proliferation of the mosquito. In addition, alerting the medical class to the symptoms of dengue, chikungunya, and zika in the interepidemic months would aid in the early detection of transmission. These actions could provide faster responses to contain transmission of these diseases and would innovate surveillance currently employed. Emergency control measures would be replaced by preventive surveillance, in which decreased infestation would result in lower incidences in epidemic periods.

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