Low completion rate of hepatitis B vaccination in female sex workers

Objective: to assess predictive factors for noncompletion of the hepatitis B vaccination schedule in female sex workers in the city of Teresina, Northeastern Brazil. Method: 402 women were interviewed and, for those who did not wish to visit specialized sites, or did not know their hepatitis B vaccination status, the vaccine was offered at their workplaces. Biand multivariate analyses were performed to identify potential predictors for noncompletion of the vaccination schedule. Results: of the 284 women eligible for vaccination, 258 (90.8%) received the second dose, 157/258 (60.8%) and 68/258 (26.3%) received the second and third doses, respectively. Working at clubs and consuming illicit drugs were predictors for noncompletion of the vaccination schedule. Conclusion: the high acceptability of the vaccine’s fi rst dose, associated with low completion rates of the vaccination schedule in sex workers, shows the need for more persuasive strategies that go beyond offering the vaccine at their workplaces. Descriptors: Sex workers; Immunization; Hepatitis B; Women; Vulnerable Populations. RESUMO Objetivo: avaliar fatores preditores de não completude do esquema vacinal contra hepatite B em mulheres que se prostituem em Teresina, Nordeste do Brasil. Método: Um total de 402 mulheres foi entrevistado e, para as que se negaram a irem a lugares especializados, ou desconheciam sua situação vacinal contra hepatite B, a vacina foi oferecida no local do trabalho. Análises bi e multivariadas foram realizadas para identifi car potenciais preditores de não completude do esquema vacinal. Resultados: Das 284 mulheres elegíveis para vacinação, 258 (90,8%) receberam a primeira dose, 157/258 (60,8%) e 68/258 (26,3%) receberam a segunda e terceira doses. Trabalhar em boates e consumir drogas ilícitas foram preditores de não completude do esquema vacinal (p<0,05). Conclusão: A elevada aceitabilidade da primeira dose da vacina, associada à baixa completude do esquema vacinal em profi ssionais do sexo, evidencia a necessidade de estratégia mais persuasiva que vá além da oferta da vacina no local de trabalho. Descritores: Profi ssionais do Sexo; Imunização; Hepatite B; Mulheres; População Vulnerável. RESUMEN Objetivo: Evaluar factores predictores del no completamiento del esquema de vacunación contra la hepatitis B en mujeres que se prostituyen en Teresina, noreste de Brasil. Método: Fueron entrevistadas 402 mujeres. Para las que se negaron a ir a lugares especializados o desconocían su situación de vacunación contra la hepatitis B, la vacuna fue ofrecida en lugar de trabajo. Fueron efectuados análisis multivariados para identifi car potenciales predictores del no completamiento del esquema de vacunación. Resultados: de las 284 mujeres elegibles para vacunación, 258 (90,8%) recibieron primera dosis, 157/258 (60,8%) y 68/258 (26,3%) recibieron segunda y tercera dosis. Trabajar en burdeles y consumir drogas fueron factores predictores de no completamiento del esquema (p<0,05). Conclusión: La elevada aceptación de la primera dosis, asociada al bajo completamiento del esquema de vacunación en profesionales del sexo, evidencia necesidad de una estrategia más persuasiva, más allá de la oferta de vacunación en el lugar de trabajo. Descriptores: Trabajadores Sexuales; Inmunización; Hepatitis B; Mujeres; Poblaciones Vulnerables. Low completion rate of hepatitis B vaccination in female sex workers Baixa completude da vacina contra hepatite B em mulheres profi ssionais do sexo Esquema incompleto de vacunación contra hepatitis B en mujeres profesionales del sexo Rosilane de Lima Brito Magalhães E-mail: rosilane@ufpi.edu.br CORRESPONDING AUTHOR


Low completion rate of hepatitis B vaccination in female sex workers
Baixa completude da vacina contra hepatite B em mulheres profi ssionais do sexo Esquema incompleto de vacunación contra hepatitis B en mujeres profesionales del sexo Rosilane de Lima Brito Magalhães E-mail: rosilane@ufpi.edu.br

CORRESPONDING AUTHOR
Because this is a difficult population to find, the snowball technique was employed in order to obtain participants (16) .Thus, initially, through the APROSPI, five key-FSWs were contacted and invited to participate in the study.These women worked at different parts of the city of Teresina.They were asked to invite other women who, in turn, would invite their peers and so on, until reaching the desired sample size.
All participants were interviewed for sociodemographic (age, education, marital status and work location) and behavioral data [(number of sexual partners/week, use of condom during sexual intercourse, tattoos and/or body piercings, prior history of drug use and prior history of sexually transmitted diseases (STDs)], in addition to information on prior vaccinations.Interviews took place at a private site previously agreed upon by the research team and participants, and they were conducted by a previously trained team.In case participants were eligible according to the interview, the first dose of the hepatitis B vaccine was offered.The following doses were scheduled at times and days chosen by the participants.After three unsuccessful scheduled vaccinations, they were considered lost to follow-up.
The variable for conclusion of the study was completion of the three hepatitis B vaccine doses.Predictive variables were: age, education, stable partnership, another work activity, place of prostitution, presence of tattoos and/or body piercings, prior drug use, use of condoms during sexual intercourse, number of sexual partnerships and history of STDs.
The vaccine employed in the study was the VrHB-IB ® , produced by the Butantan Institute and available at public health services.The vaccine was administered intramuscularly at the deltoid muscle, in three doses (1 mL/dose), at 30 and 150-day intervals; between the first and second doses, and second and third doses, respectively (17) .

Analysis of results and statistics
Interview data and adherence to vaccination were coded and doubly entered in a Microsoft ® Excel for Windows 2007 spreadsheet.All data were then exported to the IBM ® SOSS ® 15.0 software.Descriptive statistical analysis was then conducted, with absolute frequency, relative frequency, mean, median and standard deviation (SD) values estimated.The chi-squared test and Student's t-test were employed to analyze differences between proportions and means, respectively.Variables that presented p-values <0.10 were included in a backward logistic regression model.Variables with p-values <0.05 were considered statistically significant.

RESULTS
A total of 402 female sex workers in Teresina, state of Piauí, Brazil, participated in the study.Their mean age was 31.3 years (SD = 9.6) (Table 1).Of all FSWs, 2.7% reported having over 11 years of education, 29.4% from 9 to 11 years, 45.8% from 5 to 8 years, 12.7% from 1 to 4 years and the remaining (9.5%) never attended school.Most (71.9%) reported monthly incomes close to one minimum wage (from R$ 600.00 to R$ 1,000.00).As for marital status, 232 (57.7%) reported having partners.
Almost half of the women (45.5%) worked at squares and bars in the city, 36.8% at brothels and 17.7% at clubs/show houses.

INTRODUCTION
The hepatitis B virus (HBV) can cause acute and/or chronic hepatitis B and its complications, such as cirrhosis and hepatocellular carcinoma (1) .Globally, around two billion people have already been infected with this virus and 240 million are chronic carriers (2)(3) .In Brazil, where hepatitis B endemicity is low (4) , a higher prevalence for this infection has been observed in more vulnerable populations, such as sex workers (5)(6) .
The hepatitis B vaccine is the most effective measure for prevention.In Brazil, since the end of the 90s, that measure has been part of the vaccination calendar for children and also for some specific population groups, such as sex workers.Currently, it is offered for the whole population below the age of 50 and populations at higher risk, such as sex workers, drug users and men who have sex with men (MSM) (8) .Despite this policy, hepatitis B vaccination coverage is still low among its target demographics (5,(9)(10)(11)(12) .Thus, some strategies have been suggested for this population subgroups, such as the use of accelerated schedules and vaccination at the workplace (13)(14) .
The objective of this study was to assess predictive factors for noncompletion of the hepatitis B vaccination schedule in female sex workers in the Teresina, Northeastern Brazil.

METHOD Ethical aspects
The research project was approved by the local Human Research Ethics Committee of the Federal University of Piauí.

Study setting and design
A cross-sectional, analytical study was conducted from March 2012 to March 2015.Participants were female sex workers from the city of Teresina, Northeastern Brazil.The vaccine's first dose was offered to everyone who declined to answer or did now know their hepatitis B vaccination status and a cohort was created to assess their schedule completion.

Population
Teresina has an estimated population of 844,245 inhabitants and an HDI of 0.751v (15) .According to the Piauí Association of Prostitutes (APROSPO, as per its acronym in Portuguese), there is an estimate of 600 sex workers in Teresina (personal communication).Thus, considering an HBV susceptibility of approximately 80% in female sex workers (FSWs) (5-6)   , with a 5% tolerable error, a 95% confidence level and 2.0 design effect, the estimated number of women to compose the sample was 350.In order to compensate for losses and refusals, 15% were added to the previous number.
Inclusion criteria were: being a FSW, aged 18 or above, without previous hepatitis B vaccination or without knowledge of their vaccination status and living in Teresina, state of Piauí.Exclusion criterion was being transsexual women.

Study protocol
Verbal reports and/or records in the vaccination card were considered when assessing previous vaccinations.
Low completion rate of hepatitis B vaccination in female sex workers Magalhães RLB, et al.
Table 2 presents the bivariate analysis of potential predictors for noncompletion of the hepatitis B vaccination schedule in female sex workers in Teresina, Northeastern Brazil.The mean age of women who did not complete the schedule was lower when compared to those who completed it (30.7 vs. 33.8years; p=0.023).In addition, higher proportions for noncompletion of vaccination schedule were observed in women who reported only prostitution as their source of income, who had body piercings, used illegal drugs and who worked at brothels (p<0.5).These variables were included in a multivariate logistic regression model (Table 3).

DISCUSSION
The studied population was composed, mostly, of young women with low education.These characteristics seem common among female sex workers in Brazil and in other countries (9,(18)(19)(20)(21)(22) .
In this study, as well as in others conducted with difficult to reach populations, adherence to the first dose was good, demonstrating this population's willingness for vaccination (9)(10)23) . Howeer, the second and, especially, the third doses challenged the health workers.In fact, almost all eligible women received the first dose of the vaccine.However, almost a third of the women did not return in the interval between the first and second doses, and practically a fourth (26.3%; 95% CI 21.36-32.05) of those who received the first dose completed the vaccination schedule, which is a worse result than the previous ones.
Despite the high frequency of missed follow-ups, especially due to the participants geographical mobility, two factors remained independently associated with noncompletion of the schedule: use of illicit drugs and working at clubs.
In the context of HIV/AIDS, studies demonstrate that use of illicit drugs is associated with lower adherence to antiretroviral treatment (25)(26) .Interestingly, a similar behavior has been observed in relation to the hepatitis B vaccination in female sex workers.This study and the one conducted in Belgium (24) found a negative effect of illicit drug use on completion of the vaccination schedule.
In Teresina, there is a high turnover of women who work at clubs and, in general, they receive higher pay per session when compared to those who work at public spaces, bars or brothels (data not presented).This may have contributed for the low completion of the vaccination schedule.Only 2.2% of women who worked at clubs received the three vaccine doses vs. 33.6% of those who worked at bars/streets and squares.A study conducted in MPS, midwestern Brazil, showed higher chance for completion of vaccination schedule for women who worked on streets or brothels, which suggests that the strategy of vaccination at the workplace reached the most vulnerable women (9) .Our results confirm this assumption.

Study limitations
The number of losses must be considered a study limitation, despite being a common limitation of studies involving followup in difficult to reach populations, such as sex workers.

Contributions to the nursing field
The identification of predictive factors in this study can guide better strategies for hepatitis B vaccination schedule completion, according to workplace and individual characteristics of female sex workers, for infection reduction, considering the good It is noteworthy that women who used illicit drugs presented a 2.19 (CI 95%: 1.11 -4.31) chance of not completing the schedule when compared to those who did not use those drugs.As for women who worked at clubs, the chance was 23.21 (95% CI: 3.08 -175.39) when compared to those who worked at streets and squares around the city.
Low completion rate of hepatitis B vaccination in female sex workers Magalhães RLB, et al.
acceptance of vaccination by this population.There is also the need for participation of nurses and other professionals, aiming to vaccinate these women at workplaces and provide guidance on the importance of completing the vaccination schedule.

CONCLUSION
Analysis of predictive factors for hepatitis B vaccination schedule completion in female sex workers in Teresina, Piauí, Brazil, enabled the knowledge that age, work location, body piercings, illicit drug use and other professional activities were related to noncompletion of the proposed vaccination schedule.
The high acceptability of the vaccine's first dose, associated with low completion of the vaccination schedule in female sex workers, shows the need for more persuasive strategies that go beyond offering the vaccine at their workplaces, also making them aware of the importance of completing the schedule, especially for drug users and those working at clubs.

FUNDING
To the STD/AIDS and Viral Hepatitis Department of the Brazilian Ministry of Health, to the United Nations Office on Drugs and Crime.Agreement letter 130/2013.

Table 1 -
Sociodemographic characteristics of 402 female sex workers in Teresina, Piauí, Brazil Figure 1 -Flowchart of hepatitis B vaccination in female sex workers in Teresina, Piauí, Brazil

Table 2 -
Bivariate analysis of potential predictive factors for noncompletion of the three doses of hepatitis B vaccine in female sex workers in Teresina, Piauí, Brazil

Table 3 -
Multivariate analysis of potential predictive factors for noncompletion of the three doses of hepatitis B vaccine in female sex workers in Teresina, Piauí, Brazil