ABSTRACT

Objective:

To analyze the factors associated with the individual use of insect repellent by women of childbearing age living in area endemic for arboviruses in Fortaleza, Brazil.

Methods:

This is a cohort study carried out between 2018 and 2019 with women aged between 15 and 39 years in Fortaleza, state of Ceará, Brazil. A total of 1,173 women users of one of the four selected primary health care units participated in the study. The outcome was divided into: continued use, discontinued use, and nonuse of insect repellent. Crude and adjusted multinominal logistic regression analysis was carried out guided by a hierarchical model, with presentation of the respective odds ratio (OR) and 95% confidence intervals (95%CI). The independent variables include: socioeconomic and demographic data, environmental and sanitary characteristics, knowledge of the insect repellent, and behavioral and pregnancy-related aspects.

Results:

Only 28% of the participants reported using insect repellent during the two waves of the cohort. Women with higher education (OR=2.55; 95%CI 1.44–4.51); who are employed (OR=1.51; 95%CI 1.12–2.03); who received guidance from healthcare professionals (OR=1.74; 95%CI 1.28–2.36) and the media (OR=1.43; 95%CI 1.01–2.02); who intensified precautions against mosquitoes during the epidemic (OR=3.64; 95%CI 2.29–5.78); and who were pregnant between 2016 and 2019 (OR=2.80; 95%CI 1.83–4.30) had increased odds for continued use of insect repellent.

Conclusion:

The use of insect repellent among women of childbearing age was associated with a higher level of education, employment, guidance on insect repellent provided by healthcare professionals and the media, behavioral changes to protect against mosquitoes during the Zika virus epidemic, and pregnancy when occurring as of the beginning of the epidemic period.

Keywords:
Public health; Arboviruses; Zika virus; Women’s health; Insect repellents; Vulnerable populations

INTRODUCTION

Arboviruses, including Dengue, Chikungunya, and Zika viruses, are major current threats to public health in tropical and subtropical areas, affecting about four billion people¹1. Balakrishnan VS. WHO launches global initiative for arboviral diseases. Lancet Microbe 2022; 3(6): e407. https://doi.org/10.1016/S2666-5247(22)00130-6
https://doi.org/10.1016/S2666-5247(22)00... . The global increase in the frequency and magnitude of arbovirus outbreaks has been driven by the convergence of ecological factors, including climate change²2. Liu-Helmersson J, Brännström Å, Sewe MO, Semenza JC, Rocklöv J. Estimating past, present, and future trends in the global distribution and abundance of the arbovirus vector aedes aegypti under climate change scenarios. Front Public Health 2019; 7: 148. https://doi.org/10.3389/fpubh.2019.00148
https://doi.org/10.3389/fpubh.2019.00148... ,³3. Kraemer MUG, Reiner RC, Brady OJ, Messina JP, Gilbert M, Pigott DM, et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol 2019; 4(5): 854-63. https://doi.org/10.1038/s41564-019-0376-y
https://doi.org/10.1038/s41564-019-0376-... , and socioeconomic factors⁴4. Ali S, Gugliemini O, Harber S, Harrison A, Houle L, Ivory J, et al. Environmental and social change drive the explosive emergence of zika virus in the Americas. PLoS Negl Trop Dis 2017; 11(2): e0005135. https://doi.org/10.1371/journal.pntd.0005135
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These arboviruses have caused high morbidity and mortality, with a special impact in the Americas⁵5. Jones R, Kulkarni MA, Davidson TMV, Talbot B, RADAM-LAC Research Team. Arbovirus vectors of epidemiological concern in the Americas: A scoping review of entomological studies on Zika, dengue and chikungunya virus vectors. PLoS One 2020; 15(2): e0220753. https://doi.org/10.1371/journal.pone.0220753
https://doi.org/10.1371/journal.pone.022... . Brazil is one of the most affected countries with records of several Dengue epidemics in its history and, in recent years, it has been the center for Chikungunya and Zika⁶6. Donalisio MR, Freitas ARR, Von Zuben APB. Arboviroses emergentes no Brasil: desafios para a clínica e implicações para a saúde pública. Rev Saude Publica 2017; 51: 30. https://doi.org/10.1590/S1518-8787.2017051006889
https://doi.org/10.1590/S1518-8787.20170... ,⁷7. Paixão ES, Teixeira MG, Rodrigues LC. Zika, chikungunya and dengue: the causes and threats of new and re-emerging arboviral diseases. BMJ Glob Health 2018; 3(Suppl 1): e000530. https://doi.org/10.1136/bmjgh-2017-000530
https://doi.org/10.1136/bmjgh-2017-00053... .

Socioeconomically vulnerable populations are more prone to mosquito-borne diseases due to precarious housing and basic sanitation infrastructure, failures in garbage collection, low access to information and healthcare services, low level of education, among other factors that hinder the practice of healthy actions and personal care, contributing to the permanence of these diseases⁸8. Causa R, Ochoa-Díaz-López H, Dor A, Rodríguez-León F, Solís-Hernández R, Pacheco-Soriano AL. Emerging arboviruses (dengue, chikungunya, and Zika) in Southeastern Mexico: Influence of socio-environmental determinants on knowledge and practices. Cad Saude Publica 2020; 36(6): e00110519. https://doi.org/10.1590/0102-311X00110519
https://doi.org/10.1590/0102-311X0011051... ,⁹9. Programa das Nações Unidas para o Desenvolvimento. Uma avaliação do impacto socioeconômico do virus zika na America Latina e Caribe: Brasil, Colômbia e Suriname como estudos de caso [Internet]. Nova York: Programa das Nações Unidas para o Desenvolvimento; 2017 [cited on Feb. 02, 2020]. Available at: https://www.undp.org/sites/g/files/zskgke326/files/migration/br/UNDP-RBLAC-Zika-07-20-2017-Portuguese-WEB.pdf.
https://www.undp.org/sites/g/files/zskgk... . The Zika virus (ZIKV) epidemic in 2015, both nationally and internationally¹⁰10. Brasil. Ministério da Saúde. Gabinete do Ministro. Portaria no 1.813, de 11 de novembro de 2015. Declara Emergência em Saúde Pública de importância Nacional (ESPIN) por alteração do padrão de ocorrência de microcefalias no Brasil [Internet]. Brasília: Ministério da Saúde; 2015 [cited on June 16, 2019]. Available at: https://bvsms.saude.gov.br/bvs/saudelegis/gm/2015/prt1813_11_11_2015.html
https://bvsms.saude.gov.br/bvs/saudelegi... ,¹¹11. World Health Organization. WHO Director-General summarizes the outcome of the Emergency Committee regarding clusters of microcephaly and Guillain-Barré syndrome [Internet]. 2016 [cited on Apr. 15, 2020]. Available at: https://www.who.int/en/news-room/detail/01-02-2016-who-director-general-summarizes-the-outcome-of-the-emergency-committee-regarding-clusters-of-microcephaly-and-guillain-barré-syndrome
https://www.who.int/en/news-room/detail/... , highlighted these socioeconomic-environmental determinants when it mainly affected low-income, lower-educated, black women residents of peripheral regions of the Brazilian Northeast⁹9. Programa das Nações Unidas para o Desenvolvimento. Uma avaliação do impacto socioeconômico do virus zika na America Latina e Caribe: Brasil, Colômbia e Suriname como estudos de caso [Internet]. Nova York: Programa das Nações Unidas para o Desenvolvimento; 2017 [cited on Feb. 02, 2020]. Available at: https://www.undp.org/sites/g/files/zskgke326/files/migration/br/UNDP-RBLAC-Zika-07-20-2017-Portuguese-WEB.pdf.
https://www.undp.org/sites/g/files/zskgk... ,¹²12. Albuquerque MFPM, Souza WV, Araújo TVB, Braga MC, Miranda-Filho DB, Ximenes RAA, et al. Epidemia de microcefalia e vírus Zika: a construção do conhecimento em epidemiologia. Cad Saúde Pública 2018; 34(10): e00069018. https://doi.org/10.1590/0102-311X00069018
https://doi.org/10.1590/0102-311X0006901... .

The possibility of sexual and vertical transmission of ZIKV increased the risk of the disease and, as a result, personal and household care guidelines were intensified and aimed mainly at pregnant and/or childbearing women, who were the focus of attention during the epidemic¹³13. Garcia LP. Epidemia do vírus zika e microcefalia no Brasil: emergência, evolução e enfrentamento. Rio de Janeiro: Instituto de Pesquisa Econômica Aplicada; 2018.,¹⁴14. World Health Organization. Prevention of sexual transmission of Zika virus: interim guidance update [Internet]. Geneva: WHO; 2016 [cited on May 25, 2020]. Available at: https://apps.who.int/iris/handle/10665/204421
https://apps.who.int/iris/handle/10665/2... . In view of the difficulty in implementing vector control actions in the face of various socioeconomic and environmental issues and vaccine protection against arboviruses, the use of personal protection measures has become the most tangible action for the population to protect itself from diseases¹⁵15. Lima-Camara TN. Emerging arboviruses and public health challenges in Brazil. Rev Saude Publica 2016; 50: 36. https://doi.org/10.1590/S1518-8787.2016050006791
https://doi.org/10.1590/S1518-8787.20160... ,¹⁶16. Navarro JP, Espinosa MM, Terças-Trettel ACP, Silva JH, Schuler-Faccini L, Atanaka M. Knowledge and actions for the control of the vector Aedes aegypti in a municipality in the Legal Amazon. Rev Inst Med Trop Sao Paulo 2021; 63: e64. https://doi.org/10.1590/S1678-9946202163064
https://doi.org/10.1590/S1678-9946202163... .

The regular use of body repellent was one of the recommendations present in national and international handbooks, being directed mainly to pregnant women or those who intended to become pregnant, and especially if they lived in areas infested by Aedes aegypti¹⁷17. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Protocolo de vigilância e resposta à ocorrência de microcefalia e/ou alterações do sistema nervoso central (SNC) [Internet]. Brasília: Ministério da Saúde; 2016 [cited on Jan. 10, 2020]. Available at: https://www.ribeiraopreto.sp.gov.br/files/ssaude/pdf/zika-cartilha-protocolo-microcefalia.pdf
https://www.ribeiraopreto.sp.gov.br/file... ,¹⁸18. World Health Organization. Vector control operations framework for zika virus. Geneva: World Health Organization; 2016..

Due to the epidemic scenario, in April 2016, the Brazilian government instituted the monthly distribution of two bottles of topical insect repellents to pregnant women in situations of socioeconomic vulnerability assisted by healthcare units¹⁹19. Brasil. Presidência da República. Secretaria-Geral. Subchefia para Assuntos Jurídicos. Decreto no 8.716, de abril de 2016. Institui o programa de prevenção e proteção individual de gestantes em situação de vulnerabilidade socioeconômica contra o Aedes aegypti [Internet]. Brasília: Presidência da República; 2016 [cited on June 18, 2019]. Available at: https://www.planalto.gov.br/ccivil_03/_ato2015-2018/2016/decreto/d8716.htm#:~:text=DECRETO%20N%C2%BA%208.716%2C%20DE%2020,socioecon%C3%B4mica%20contra%20o%20Aedes%20aegypti.&text=A%20PRESIDENTA%20DA%20REP%C3%9ABLICA%20%2C%20no,que%20lhe%20confere%20o%20art.
https://www.planalto.gov.br/ccivil_03/_a... . In 2018, there was an expansion of the offer to all pregnant women and the population living in endemic areas²⁰20. Brasil. Ministério da Saúde. Saúde amplia público-alvo para utilização de repelentes [Internet]. 2018 [cited on Dec. 15, 2020]. Available at: https://www.gov.br/saude/pt-br/assuntos/noticias/2018/fevereiro/saude-amplia-publico-alvo-para-utilizacao-de-repelentes
https://www.gov.br/saude/pt-br/assuntos/... . However, with the reduction in cases of microcephaly and ZIKV infections in the country, in July 2019, the action was revoked by the government in force²¹21. Brasil. Presidência da República. Secretaria-Geral. Subchefia para Assuntos Jurídicos. Decreto no 9.917, de 18 de julho de 2019. Declara a revogação, para os fins do disposto no art. 16 da Lei Complementar no 95, de 26 de fevereiro de 1998, de decretos normativos [Internet]. Brasília: Presidência da República; 2019 [cited on Oct. 22, 2019]. Available at: https://www.planalto.gov.br/ccivil_03/_ato2019-2022/2019/decreto/D9917.htm
https://www.planalto.gov.br/ccivil_03/_a... .

In view of the recommendation of the use of insect repellent as a measure of personal protection against arboviruses, which was distributed to pregnant women, and considering the absence of studies on the panorama of the use of this measure when offered to pregnant women in the state of Ceará, which concentrates high numbers of cases of Dengue, Zika, and Chikungunya, in this study we aimed to analyze the factors associated with the individual use of insect repellent by women of childbearing age living in endemic areas for arboviruses in Fortaleza, Brazil.

METHODS

Study type and location

This cohort study used data from the larger project entitled Zika em Fortaleza: resposta de uma coorte de mulheres de 15 a 39 anos (“Zika in Fortaleza: response of a cohort of women aged 15 to 39 years”) (ZIF project), carried out in the city of Fortaleza, state of Ceará, Brazil. In 2018, Fortaleza had an estimated population of 2,627,482 people with a population density of 8,373 inhabitants/km², being divided into six administrative units (Secretarias Executivas Regionais [Regional Executive Secretariats] – SER). During the study period, there were 96 Primary Health Care Units (PHCUs), and four units located in SER I, III, and V were selected (Figure 1). These regions recorded high rates of Chikungunya cases in 2017, an infection taken as a proxy for ZIKV infection²²22. Prefeitura Municipal de Fortaleza. Secretaria Municipal de Saúde. Coordenadoria de Vigilância em Saúde. Célula de Vigilância Epidemiológica. Boletim de Saúde de Fortaleza: Chikungunya 2014-2018 [Internet]. Fortaleza: Prefeitura Municipal de Fortaleza; 2019 [cited on June 18, 2019]. Available at: https://saude.fortaleza.ce.gov.br/images/BSFOR/2019/Boletim_Chikungunya_2014_2018.pdf
https://saude.fortaleza.ce.gov.br/images... .

Sample calculation

Sexually active women aged between 15 and 39 years living in Fortaleza, state of Ceará, Brazil, participated in the study. The inclusion criteria were: 1) live in the territorial area of one of the selected health care units; 2) be between 15 and 39 years of age; 3) be sexually active (at least one sexual intercourse in the last 12 months). Women aged 15 to 39 years who had undergone tubal ligation and who lived outside the selected areas were excluded from the sample.

The sample size was estimated based on the equation:

The probability of pregnancy (P) was estimated at 8.3% (+/- 2%), dividing the total number of live births in the city by the sexually active female population, aged 15 to 39 years (N), estimated at 73% of the female population in the city of Fortaleza. Considering the design effect (deff) of 2, the 95% confidence interval and a loss to follow-up (d) of 20%, it resulted in a sample size (n) of 1,752 women.

Toward the end of the collection period, there was a reduction in the recruitment rate, considering that the pregnancy rate in the study population was higher (20%) than estimated (8.3%); therefore, the baseline sample was completed with 1,496 women.

Data collection

Data collection took place in two waves. The meetings took place inside the health care units, and semi-structured questionnaires with similar questions were applied to the two waves, using the Survey Monkey software (SurveyMonkey Inc, San Mateo, California, USA). The collection period for the first wave was from February 28 to October 30, 2018; and the second wave, from February 14 to August 30, 2019.

Dependent variable

The use of insect repellent during the cohort was considered as the variable of interest, and the following questions arose: “Do you use any kind of insect repellent?”; “Is the insect repellent for individual use?”, both with yes/no answers.

Subsequently, it was categorized into three levels: “Continued use,” when the use of insect repellent was reported in both waves of the cohort; “Discontinued use,” when the use was reported in only one of the cohort waves; and “Nonuse,” when the repellent was not used in both waves of the cohort.

Independent variables

They were composed of:

• Socioeconomic and demographic factors:

  1. -

     Age group (years): variable initially continuous and later categorized into age groups: 15–19 (reference); 20–29; 30–39.

  2. -

     Race/Skin color: presented in five categories and later categorized into “white” and “non-white” (Black, mixed-race, Indigenous, Asian) (reference).

  3. -

     Level of education: based on the informed level of education, it was categorized into: Elementary school or lower (reference); Incomplete high school/Complete High school; Incomplete undergraduate/Complete undergraduate.

  4. -

     Employment status: categorized into “employed” and “unemployed” (reference).

• Environmental and sanitary characteristics of the household:

The variable presence of a backyard in the household was categorized as “yes” and “no” (reference). The variable household sewage destination was composed of: “public system/septic tank,” which are characterized as recommended sewage destinations, and “open air” (reference category).

• Received guidance on insect repellent:

The variables were based on the following questions: “Where did you receive guidance on the use of insect repellent as a protective measure?” Several means of information were presented to the participants, among them: healthcare professionals (physicians and non-physicians) and the media (the Internet and television), which were dichotomized into “yes” and “no” (reference).

• Zika-related behavioral factors:

  1. -

     Has postponed pregnancy due to the Zika epidemic: dichotomized into “ye” and “no” (reference);

  2. -

     Precaution against the disease-transmitting mosquito during the Zika epidemic: categorized as “intensified precautions against the mosquito” or “there were no behavioral changes” (reference).

• Pregnancy:

History of pregnancy before and as of the epidemic period was categorized as: pregnancy before 2016; pregnancy between 2016 and 2019; and has never gotten pregnant (reference). Childbirths/pregnancies that occurred before and from January 2016 onward were considered. This temporal demarcation was chosen because it was only after the Brazilian government declared an association between the Zika virus infection and cases of microcephaly, at the end of 2015¹³13. Garcia LP. Epidemia do vírus zika e microcefalia no Brasil: emergência, evolução e enfrentamento. Rio de Janeiro: Instituto de Pesquisa Econômica Aplicada; 2018.,²³23. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Vírus Zika no Brasil: a resposta do SUS [Internet]. Brasília: Ministério da Saúde; 2017 [cited on Oct. 04, 2020]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/virus_zika_brasil_resposta_sus.pdf
https://bvsms.saude.gov.br/bvs/publicaco... , that the use of personal protection measures for pregnant women and women of childbearing age began to be aimed at the prevention of the disease²⁴24. Brasil. Ministério da Saúde. Secretaria de Atenção à Saúde. Protocolo de atenção à saúde e resposta à ocorrência de microcefalia relacionada à infecção pelo vírus zika [Internet]. Brasília: Ministério da Saúde; 2016 [cited on Dec. 02, 2019]. Available at: https://portaldeboaspraticas.iff.fiocruz.br/wp-content/uploads/2019/02/protocolo_resposta_microcefalia_relacionada_infeccao_virus_zika.pdf
https://portaldeboaspraticas.iff.fiocruz... .

Statistical analysis

A descriptive analysis of the epidemiological profile of the participants and the characteristics of insect repellent use was performed, with presentation of the respective frequencies and confidence intervals (95%CI).

Nominal multinomial logistic regression was used to verify the associations of the independent variables with the response variable of interest, i.e., “Continued use,” “Discontinued use,” and “Nonuse” of insect repellent, the latter deemed as a reference category. The results were presented as odds ratios (OR) along with their respective 95% confidence intervals, considering a 5% significance level.

A hierarchical explanatory model was initially suggested for studies applied in other areas²⁵25. Victora CG, Huttly SR, Fuchs SC, Olinto MT. The role of conceptual frameworks in epidemiological analysis: a hierarchical approach. Int J Epidemiol 1997; 26(1): 224-7. https://doi.org/10.1093/ije/26.1.224
https://doi.org/10.1093/ije/26.1.224... . The predictor variables were grouped into five blocks, as shown in Figure 2: Block 1 – Socioeconomic and demographic factors (age group, level of education, race/skin color, employment status); Block 2 – Environmental and sanitary characteristics of the household (presence of a backyard in the household, household sewage destination); Block 3 – Received guidance on insect repellent (by healthcare professionals, through the media [television/the Internet]); Block 4 – Zika-related behavioral factors (has postponed pregnancy due to the Zika epidemic, precaution against the disease-transmitting mosquito during the Zika epidemic); Block 5 – Pregnancy (history of pregnancy before and as of the epidemic period).

Bivariate analyses were performed for all variables of the five blocks using Pearson’s chi-square hypothesis test (χ²2. Liu-Helmersson J, Brännström Å, Sewe MO, Semenza JC, Rocklöv J. Estimating past, present, and future trends in the global distribution and abundance of the arbovirus vector aedes aegypti under climate change scenarios. Front Public Health 2019; 7: 148. https://doi.org/10.3389/fpubh.2019.00148
https://doi.org/10.3389/fpubh.2019.00148... ). The socioeconomic and demographic variables (Block 1) were considered the most distal in the process of determining the use of the insect repellent. The variables of this block that were statistically significant at the 0.05 level remained in the final model. For the remaining blocks, the variables that remained significant up to 0.20 were evaluated in multinomial multivariate analysis internal to the block. The same process was repeated for the others. In the final model, all statistically significant variables were considered associated with the different uses of the insect repellent.

The Wald test was applied to evaluate the statistical relationship between the independent variable in the differentiation between the two groups and the likelihood ratio test to evaluate the overall relationship between the independent variables and the outcome. Statistical differences were compared between cohort waves for each exploratory variable using the Fisher’s exact test. The variables age group, ethnicity/skin color, and level of education were analyzed based on information provided in the 1st wave, and the variables in block 4 were investigated only in the 1st wave, being analyzed based on this information (Supplementary Table 1). All analyses were performed using the STATA™ software v. 16.

Ethical aspects

This investigation is part of a matrix project approved by the Research Ethics Committee of the Universidade Federal do Ceará (UFC), under protocol No. 2.497.069, complying with national and international ethical guidelines for research involving human beings.

RESULTS

A total of 1,496 women of childbearing age participated in the first wave, in 2018. In the second wave (2019), there was a loss to follow-up of 323 women (21.6%), totaling 1,173 participants, who were analyzed in this article.

Regarding the epidemiological profile of the participants (Table 1), most were between 20 and 29 years old (48.6%), self-reported to be mixed-race (70.3%), had incomplete high school or high school education (57.7%), and had a steady partner (60.4%). Regarding employment status, 61% were unemployed. About 78% of the women had a history of pregnancy, with the majority of pregnancies occurring between 2016 and 2019.

Regarding the use of insect repellent during the cohort, approximately 62% of the women followed the recommendation at some point during the follow-up, of which 28% reported the use of insect repellent in both waves, while 38.3% did not use it.

The main justifications for not using repellent were: “do not believe it is necessary” (37.2%); “very expensive” (22.0%); “do not like to use it” (11.5%), the latter being associated with the consistency and smell of the product. Other factors, such as “forgot to use it” (9.4%), “sloppiness/carelessness” (5.3%), were also reported. In addition, 1.6% of the women denied the current use, but reported having used it at specific times: “at times when more mosquitoes appear,” during “epidemics.” Another reported factor was “fear of using the insect repellent,” which was related to the fact that they were pregnant or because they had some underlying disease. Other justifications were related to the replacement of the insect repellent by other products, such as creams, moisturizers and sunscreen, and by mechanical methods such as fans and mosquito nets.

In Table 2 we show the bivariate analysis between the independent variables and the outcome categories. From the analysis of the blocks, the variables level of education and employment status of block 1 remained statistically significant. The variables in block 2 remained significant only for the category of discontinued use. In block 3, guidance provided by healthcare professionals and the media was significant when jointly analyzed. In block 4, only the variable precaution against the disease-transmitting mosquito during the Zika epidemic was significant for the outcome categories. Finally, in block 5, the variable history of pregnancy before and as of the epidemic period was extremely significant for the continued and discontinued use of the insect repellent.

The final model of the multinomial logistic regression is presented in Table 3. Women of childbearing age with a college degree were more likely to continue using the insect repellent (OR=2.55; 95%CI 1.44–4.51) and to discontinue its use (OR=1.77; 95%CI 1.01–3.10), in relation to those with elementary level of education or lower. Being employed had a positive impact on the use of the measure throughout the follow-up (OR=1.51; 95%CI 1.12–2.03) compared to unemployed women. Receiving guidance on insect repellent from healthcare professionals (OR=1.74; 95%CI 1.28–2.36) and the media (OR=1.43; 95%CI 1.01–2.02) had repercussions on the chances of continued use of the measure. Women who intensified their precautions against the mosquito during the epidemic had increased chances of both continued use of the insect repellent (OR=3.64; 95%CI 2.29–5.78) and the discontinued use (OR=1.86; 95%CI 1.30–2.65), compared to participants who did not change their behaviors. Pregnant women between 2016 and 2019 were more likely to continue using the repellent (OR=2.80; 95%CI 1.83–4.30) and to discontinue using it (OR=1.88; 95%CI 1.30–2.72) in relation to women who had never gotten pregnant.

DISCUSSION

Studies carried out during the ZIKV epidemic documented the relationship between the level of education in the face of behavioral changes and the population’s knowledge of the prevention of arboviruses. Authors of these studies identified that a lower level of education led to low use of recommended precautions²⁶26. Maharajan MK, Rajiah K, Belotindos JAS, Basa MS. Social determinants predicting the knowledge, attitudes, and practices of women toward zika virus infection. Front Public Health 2020; 8: 170. https://doi.org/10.3389/fpubh.2020.00170
https://doi.org/10.3389/fpubh.2020.00170... ,²⁷27. Piltch-Loeb R, Abramson DM, Merdjanoff AA. Risk salience of a novel virus: US population risk perception, knowledge, and receptivity to public health interventions regarding the Zika virus prior to local transmission. PLoS One 2017; 12(12): e0188666. https://doi.org/10.1371/journal.pone.0188666
https://doi.org/10.1371/journal.pone.018... , while a higher level of education and better economic conditions favored the adoption of personal protection measures²⁸28. Pires LC, Dantas LR, Witkin SS, Bertozzi APAP, Dezena RCAB, Rodrigues MMD, et al. Knowledge of zika virus transmission and its prevention among high-risk pregnant women in Brazil. Viruses 2021; 13(2): 242. https://doi.org/10.3390/v13020242
https://doi.org/10.3390/v13020242...

29. Cartaxo MFS, Silva SMD, Silva JGM, Beltrão EIC, Brayner FA, Lima Filho JL, et al. Social determinants of health associated with topical repellent use in pregnancy: a cross-sectional study during a Zika outbreak in Brazil. Trans R Soc Trop Med Hyg 2019; 113(2): 65-73. https://doi.org/10.1093/trstmh/try114
https://doi.org/10.1093/trstmh/try114... -³⁰30. Dantas Melo VA, Santos Silva JR, La Corte R. Use of mosquito repellents to protect against Zika virus infection among pregnant women in Brazil. Public Health 2019; 171: 89-96. https://doi.org/10.1016/j.puhe.2019.04.002
https://doi.org/10.1016/j.puhe.2019.04.0... , corroborating this research. However, approximately 9% of the participants in this survey reported having a college degree, a number far below the Brazilian level — according to which, in 2019, there were 19.4% women aged 25 years and over who had a college degree³¹31. Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional por Amostra de Domicílios Contínua. Pessoas de 25 anos ou mais de idade, por sexo e grupamentos de nível de instrução [Internet]. 2019 [cited on Nov. 10, 2023]. Available at: https://sidra.ibge.gov.br/tabela/7135
https://sidra.ibge.gov.br/tabela/7135... , demonstrating that the study participants compose a group of high social vulnerability.

In Brazil, the targeting of public policies to pregnant women during the Zika epidemic, including the delivery of insect repellent, guidance in prenatal guides, and the dissemination of information through the media¹³13. Garcia LP. Epidemia do vírus zika e microcefalia no Brasil: emergência, evolução e enfrentamento. Rio de Janeiro: Instituto de Pesquisa Econômica Aplicada; 2018.,²³23. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Vírus Zika no Brasil: a resposta do SUS [Internet]. Brasília: Ministério da Saúde; 2017 [cited on Oct. 04, 2020]. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/virus_zika_brasil_resposta_sus.pdf
https://bvsms.saude.gov.br/bvs/publicaco... , made pregnancy a prominent factor in the association with insect repellent use, as evidenced in this study. Countries affected by the ZIKV epidemic also highlighted this finding. Authors of a research conducted in Puerto Rico during the epidemic period found that pregnant women were 1.44 times more likely to use insect repellent than nonpregnant women³²32. Ellington SR, Simeone RM, Serrano-Rodriguez RA, Bertolli J, Swartzendruber A, Goldberg HI, et al. Zika prevention behaviors among women of reproductive age in Puerto Rico, 2016. Am J Prev Med 2021; 61(3): e149-e155. https://doi.org/10.1016/j.amepre.2021.03.004
https://doi.org/10.1016/j.amepre.2021.03... . In the Virgin Islands, there was a high rate of adherence to insect repellent by pregnant women (74%), who received educational materials and home and personal protection resources, including insect repellent³³33. Prue CE, Roth Jr JN, Garcia-Williams A, Yoos A, Camperlengo L, DeWilde L, et al. Awareness, beliefs, and actions concerning zika virus among pregnant women and community members – U.S. Virgin Islands, November–December 2016. MMWR Morb Mortal Wkly Rep 2017; 66(34): 909-13. https://doi.org/10.15585/mmwr.mm6634a4
https://doi.org/10.15585/mmwr.mm6634a4... .

In this cohort, despite the strong association between pregnancy and insect repellent use, we observed a low percentage of continued repellent use by pregnant women between 2016 and 2019, compared to that found in the Virgin Islands. It is also noteworthy that 29% of these pregnant women did not adhere to the measure despite receiving the product free of charge during the period, suggesting flaws in the guidance on the supply and use of the insect repellent, in addition to other justifications for nonuse found in this study.

The participants of the research, pregnant and nonpregnant, evidenced as the main justifications for nonadherence the insufficient knowledge of the repellent and the financial aspect linked to its acquisition. During the ZIKV epidemic, the prevention of the disease entailed costs for women, leading the poorest to put aside practices that required financial expenditure³⁰30. Dantas Melo VA, Santos Silva JR, La Corte R. Use of mosquito repellents to protect against Zika virus infection among pregnant women in Brazil. Public Health 2019; 171: 89-96. https://doi.org/10.1016/j.puhe.2019.04.002
https://doi.org/10.1016/j.puhe.2019.04.0... ,³⁴34. Stolow J, Kendall C, Pinheiro FML, Feitosa MCR, Furtado KAA, Martins AF, et al. Women’s perceptions of zika virus prevention recommendations in Fortaleza, Brazil. J Prev Health Promot 2020; 1(2): 288-314. https://doi.org/10.1177/2632077020970875
https://doi.org/10.1177/2632077020970875... . This is the case of insect repellents, which, when not offered free of charge, implies additional costs for the family.

According to Dorsett et al.³⁵35. Dorsett C, Oh H, Paulemond ML, Rychtář J. Optimal repellent usage to combat dengue fever. Bull Math Biol 2016; 78(5): 916-22. https://doi.org/10.1007/s11538-016-0167-z
https://doi.org/10.1007/s11538-016-0167-... , the voluntary use of insect repellent would not lead to the eradication of the disease; however, when its access is enabled and expanded, either at more affordable costs or distributed free of charge, its effectiveness increases and provides greater protection to the community.

Taking this into consideration, the discontinuity of the insect repellent supply policy in Brazil in 2019 will impact access to the measure, especially by the most disadvantaged women, increasing the risk of exposure to the virus and the possibility of new epidemics. The end of the insect repellent distribution policy occurred one month before the end of the cohort’s data collection, making it impossible to analyze the impact on access to the measure after this period.

Accessing the product does not warrant its use. In this study, guidance provided by healthcare professionals and the media favored the use of insect repellent, a fact also evidenced in other studies²⁸28. Pires LC, Dantas LR, Witkin SS, Bertozzi APAP, Dezena RCAB, Rodrigues MMD, et al. Knowledge of zika virus transmission and its prevention among high-risk pregnant women in Brazil. Viruses 2021; 13(2): 242. https://doi.org/10.3390/v13020242
https://doi.org/10.3390/v13020242... ,³⁰30. Dantas Melo VA, Santos Silva JR, La Corte R. Use of mosquito repellents to protect against Zika virus infection among pregnant women in Brazil. Public Health 2019; 171: 89-96. https://doi.org/10.1016/j.puhe.2019.04.002
https://doi.org/10.1016/j.puhe.2019.04.0... . Conversely, the information only seemed to make a difference for a portion of the women exposed to the recommendations. Authors of a study conducted in Colombia between 2017 and 2018 identified a high level of knowledge of Zika and its forms of transmission among pregnant women; nonetheless, these factors did not result in an impact on changing behavior and adherence to protective measures³⁶36. Burkel VK, Newton SM, Acosta J, Valencia D, Benavides M, Tong VT, et al. Zika virus knowledge, attitudes and prevention behaviors among pregnant women in the ZEN cohort study, Colombia, 2017–2018. Trans R Soc Trop Med Hyg 2023; 117(7): 496-504. https://doi.org/10.1093/trstmh/trad005
https://doi.org/10.1093/trstmh/trad005... .

The provision of guidance without considering the characteristics of the target audience, behavioral changes, and the application of advances in the theory and practice of health communication²⁷27. Piltch-Loeb R, Abramson DM, Merdjanoff AA. Risk salience of a novel virus: US population risk perception, knowledge, and receptivity to public health interventions regarding the Zika virus prior to local transmission. PLoS One 2017; 12(12): e0188666. https://doi.org/10.1371/journal.pone.0188666
https://doi.org/10.1371/journal.pone.018... ,³⁴34. Stolow J, Kendall C, Pinheiro FML, Feitosa MCR, Furtado KAA, Martins AF, et al. Women’s perceptions of zika virus prevention recommendations in Fortaleza, Brazil. J Prev Health Promot 2020; 1(2): 288-314. https://doi.org/10.1177/2632077020970875
https://doi.org/10.1177/2632077020970875... is reflected in low adherence to the measure or irregular use, even when a preventive strategy is accessed²⁸28. Pires LC, Dantas LR, Witkin SS, Bertozzi APAP, Dezena RCAB, Rodrigues MMD, et al. Knowledge of zika virus transmission and its prevention among high-risk pregnant women in Brazil. Viruses 2021; 13(2): 242. https://doi.org/10.3390/v13020242
https://doi.org/10.3390/v13020242... ,²⁹29. Cartaxo MFS, Silva SMD, Silva JGM, Beltrão EIC, Brayner FA, Lima Filho JL, et al. Social determinants of health associated with topical repellent use in pregnancy: a cross-sectional study during a Zika outbreak in Brazil. Trans R Soc Trop Med Hyg 2019; 113(2): 65-73. https://doi.org/10.1093/trstmh/try114
https://doi.org/10.1093/trstmh/try114... ,³⁷37. Ruben BD. Communication theory and health communication practice: the more things change, the more they stay the same. Health Commun 2016; 31(1): 1-11. https://doi.org/10.1080/10410236.2014.923086
https://doi.org/10.1080/10410236.2014.92... .

It should be noted that after the drop in Zika cases and births of children with congenital syndromes related to the Zika virus, there was a reduction in the spread of guidelines to combat arboviruses. Nevertheless, the coping with the Sars-Cov-2 pandemic situation in 2020 camouflaged the attention to arboviruses³⁸38. Azevedo C. Pandemia pode mascarar casos de arboviroses, indica seminário [Internet]. Rio de Janeiro: Fundação Oswaldo Cruz; 2021 [cited on July 14, 2022]. Available at: https://portal.fiocruz.br/noticia/pandemia-pode-mascarar-casos-de-arboviroses-indica-seminario
https://portal.fiocruz.br/noticia/pandem... , causing an underreporting of cases and relaxation of public health measures.

Given this scenario, Brazil has been registering an increase in cases of Dengue, Chikungunya, and Zika³⁹39. Brasil. Ministério da Saúde. Secretária de Vigilância em Saúde. Monitoramento dos casos de arboviroses até a semana epidemiológica 31 de 2022 [Internet]. Boletim Epidemiológico 2022; 53 [cited on Nov. 08, 2022]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/boletins/epidemiologicos/edicoes/2022/boletim-epidemiologico-vol-53-no30.pdf
https://www.gov.br/saude/pt-br/centrais-... ,⁴⁰40. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Monitoramento das arboviroses urbanas: semanas epidemiológicas 1 a 35 de 2023 [Internet]. Boletim Epidemiológico 2023; 54. [cited on Dec. 01, 2023]. Available at: https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/boletins/epidemiologicos/edicoes/2023/boletim-epidemiologico-volume-54-no-13#:~:text=No%20per%C3%ADodo%20compreendido%20entre%20a,18.564%20de%20DSA%20e%20DG
https://www.gov.br/saude/pt-br/centrais-... . The increase in cases linked to the socioeconomic conditions of the population aggravated by the COVID-19 pandemic could turn Zika and other arboviruses into a true social, economic, and public health disaster in the country, if they are not prevented and controlled.

This study has limitations, among them the homogeneity of the sample, which, due to the purposes of the study, does not enable to extrapolate the data to groups with greater socio-environmental and economic advantage. Furthermore, there may be biases of loss to follow-up that occurred in the second wave, even after attempts to contact them through telephone calls and support from health agents. We identified statistical differences between the waves for the variables employment status and guidance provided by healthcare professionals and the media. In addition to the losses to follow-up, we understand that Brazil’s economic instability was reflected in the high unemployment rates, which were aggravated during the cohort period. Regarding the guidelines for the use of insect repellent, there was a decrease in the dissemination of information as it was distancing itself at the beginning of the epidemic, causing differences between the waves of the cohort. Moreover, the collected pieces of information were self-reported by the participants, and there may be memory biases; in order to minimize them, we used recall methods during the interview, and the participants were reminded of the years related to the epidemic and related events. Finally, the identification of the use of insect repellent did not consider the frequency of applications, and it was not possible to guarantee that it occurred according to the product’s recommendations⁴¹41. Tavares M, Silva MRM, Siqueira LBO, Rodrigues RAS, Bodjolle-d’Almeira L, Santos EP, et al. Trends in insect repellent formulations: a review. Int J Pharm 2018; 539(1-2): 190-209. https://doi.org/10.1016/j.ijpharm.2018.01.046
https://doi.org/10.1016/j.ijpharm.2018.0... .

Despite these limitations, this study has the potential to support further research by presenting relevant findings and guiding government agencies in the formulation of public policies for the prevention of arboviruses. By adopting the cohort design, we identified factors that influence, over time, the use of insect repellent as a measure of personal protection among women of childbearing age, pregnant and nonpregnant.

All in all, we conclude this study by stating that the use of insect repellent as a measure of personal protection among women of childbearing age was associated with a higher level of education, employment, guidance provided by healthcare professionals and the media, and especially pregnancy and behavioral changes aimed at precaution against Zika and other arboviruses. However, the socioeconomic profile linked to the use of the measure does not represent a large portion of the Brazilian population, making it necessary to strengthen public policies that guarantee access to education, services and recommended means of personal and home protection. Taking this into consideration, we recommend the provision of insect repellent to women of childbearing age, living in endemic areas and with low socioeconomic status, combined with the provision of safe and reliable guidance, using an accessible language and which is feasible to the reality of these women and families, in order to strengthen knowledge and adherence to the measure and mitigate the high risk of exposure to the virus.

ACKNOWLEDGMENTS

The authors would like to thank the funding agencies CNPq, CAPES and FUNCAP, which made the execution of this project feasible and for providing funding for the scholarships of students and researchers. To the women participating in the research, the main reason for this study.

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