Journal of Medical Virology

Human Papillomavirus: Prevalence and Factors Associated in Women Prisoners Population From the Eastern Brazilian Amazon Sylvia Regina Vasconcellos de Aguiar,1 Fabiola Elizabeth Villanova,1 Luisa Carı´cio Martins,1 Milena Silva dos Santos,1 Juliana de Paula Maciel,1 Luiz Fa´bio Magno Falca˜o,1,2 Hellen Thais Fuzii,1 and Juarez Antoˆnio Simo˜es Quaresma1,2* 1 2

Federal University of Para´, Bele´m, Para´, Brazil Center of Biological and Health Sciences, University of the State of Para´, Bele´m, Para´, Brazil

This study aimed to examine the prevalence of human papillomavirus (HPV) and the associated factors among female prisoners in Ananindeua City, State of Para´, Brazil. In 2010, 190 cervical samples were obtained, and Pap smear and polymerase chain reaction (GE Health CareTM, Uppsala, Sweden) were performed. Additionally, a questionnaire was used. The prevalence of HPV was 10.5%, and the presence of cervical intraepithelial neoplasia grade I (n ¼ 33, 17.5%; P < 0.1) was associated with HPV infection. The presence of lowgrade squamous intraepithelial lesions was greater in women with HPV than in those without HPV infection, indicating that HPV infection is a risk factor for such injuries and that viral screening and prevention are extremely important in public health among female prisoners in Amazon. J. Med. Virol. # 2014 Wiley Periodicals, Inc.

KEY WORDS:

human papillomavirus; epidemiology; prisoners; Amazon

INTRODUCTION Human papillomavirus (HPV) infection is the most prevalent sexually transmitted disease (STD) worldwide, and with 137,000 new cases annually in Brazil [Rocha et al., 2013]. Although, HPV infection is not sufficient to cause squamous intraepithelial lesion development, 90% of women with cervical cancer are positive for HPV infection, and the occurrence of cervical lesions is concentrated in the Amazon region [De Oliveira et al., 2013; Lorenzi et al., 2013]. Between 2000 and 2010, the population of female prisoners has increased considerably in Brazil (135.4%). This value is threefold higher than the C 2014 WILEY PERIODICALS, INC. 

increase in the population of male prisoners (53.4%) and has resulted in serious national public health problems. Factors such as a low socioeconomic profile, which is associated with dangerous confinement conditions and lack of public health policies, make this population more vulnerable to various infections, including HPV [Pinto et al., 2011; Zonta et al., 2012]. Furthermore, the distribution and factors associated with lesions of the cervix, including HPV infection, are not well characterized in certain regions and population groups in Brazil, such as the Amazon and prison populations. This paper reports the prevalence of genital HPV infection and its possible relation to cervical lesions in women prisoners of the eastern Brazilian Amazon. Other factors related to HPV infection are also described. MATERIALS AND METHODS Study Setting and Study Subjects The study was conducted in the eastern Brazilian Amazon at the Center for Women’s Re-education in the metropolitan area of the city of Ananindeua, which has approximately 471,744 inhabitants. This rehabilitation center is the only women’s prison in the state of Para´ and receives women offenders from various cities and other states as well as foreign women prisoners. It has the capacity to hold 480 prisoners, but currently houses 610 women of different ages who have committed different types of

Conflict of Interest: None.  Correspondence to: Juarez Antoˆnio Simo˜es Quaresma, Nu´cleo de Medicina Tropical, Universidade Federal do Para´, Avenida Generalı´ssimo Deodoro, 92 Bele´m, Para´ 66055-240, Brazil. E-mail: [email protected] Accepted 4 April 2014 DOI 10.1002/jmv.23972 Published online in Wiley Online Library (wileyonlinelibrary.com).

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de Aguiar et al.

crime, such as theft, drug trafficking, and murder. Overcrowding, adverse structural conditions and insecurity in the health-care of inmates and the scarcity of prevention, early detection, and treatment programmes contribute to the increased incidence and prevalence of diseases in general, especially STDs [Pinto et al., 2011]. Study Type and Sample Calculation This study was performed as a transverse, analytical, population-based study. To calculate the sample size, the overall prevalence of genital infection by any type of HPV in Brazilian women in the age range of 18–60 years was considered to be 25%, according to studies by Franco et al. [1999]. The power of the test was 80%, the confidence interval was 95%, and the alpha level was 5%. Accordingly, an estimated sample value of 185 women was calculated. Data Collection The study participants were selected from among sexually active adult women who attended the Center for Women’s Re-Education Clinic for consultation and routine nursing procedures, such as examination for the prevention of cancer of the cervix (PCC), between January 2008 and March 2010. Initially, 210 women were screened, but only 190 had cervical material suitable for molecular testing for HPV. A questionnaire was administered prior to the gynaecological consultation, which was divided into the following parts: demographic and behavioral information, sexual information, contraceptive information, reproductive information, gynaecological information, and laboratory data (test results). These data were collected to identify variables possibly associated with HPV infection. Sample Collection and Analysis Cervical samples were collected by a nurse and obtained by scraping the ectocervix with an Ayerstype spatula (AdlinTM, Jaragua do Sul, Brazil) and brushing the endocervix with a Campos da Paz-type brush (AdlinTM Jaragua do Sul, Brazil); both tools were disposable. Samples were divided into two portions, one of which was used for conventional cytological light microscopy evaluation (Papanicolaou test) and the other for molecular biological testing. The Papanicolaou test was performed by a medical cytopathologist and the molecular biology tests were performed at the Laboratory of Immunopathology of the Center for Tropical Medicine, Federal University of Para´, Bele´m, PA. To verify the presence of viral DNA, the cervical cell samples obtained during collection were immersed in 15-ml polyethylene tubes that were properly identified with codes. The tubes contained 5 ml of phosphate-buffered saline (PBS), and the samples were immediately stored at 20˚C. At the end of the daily collections, the biological materiJ. Med. Virol. DOI 10.1002/jmv

als were transported in a sealed Styrofoam box with ice to the Laboratory of Immunology at the Tropical Medicine Centre. These samples were then centrifuged at 150g for 5 min to precipitate the cervical cells, to which 200 ml of PBS was added subsequently; the cells were stored at 20˚C. DNA extraction was performed using the GFX kit (GE Health Care TM, Uppsala, Sweden), and the polymerase chain reaction method (PCR; GE Health CareTM) was used for analysis. Statistical Analysis All collected information was organized using the ExcelTM 2007 software package (Microsoft Corporation, Redmond, WA). Statistical analyses were conducted using the programs BIO ESTATTM, version 5.0 (Civil Society Mamiraua´, Manaus, Brazil) and Epi InfoTM, version 3.5.1 (Centers for Disease Control and Prevention, Atlanta, GA). A univariate analysis was used to determine the prevalence of HPV infection, the absolute and relative frequencies of the qualitative variables, and measurements of central tendencies and dispersion. Factors associated with HPV infection were investigated in a bivariate analysis. The prevalence odds ratios (PR) were calculated with confidence intervals (CI) of 95%. Statistical significance was tested using the Fisher’s Exact test, and an a level ¼ 0.05 was adopted to reject the null hypothesis. Ethical Aspects The present study was approved by the ethical committee of the Tropical Medicine Centre, Federal University of Para´ (Protocol No. 036/2009). Research Involving Human Beings rules and their complementary of the National Health Council/Ministry of Health of Brazil (Res. 196/96) was complied based on the Declaration of Helsinki guidelines of 1975, revised in 1983. RESULTS The Pap tests showed that all collected cervical materials were of good quality. PCR or nested PCR was used to detect the presence of viral HPV in 10.5% (n ¼ 20) of the analyzed samples (Table I). The mean age of the women was 30.5  9 years (median, 28 years; range, 18–60 years). Factors such as the marital status (P ¼ 0.07), educational level (P ¼ 0.55), tobacco use (P ¼ 0.55 and P ¼ 0.86), average age at sexual initiation (P ¼ 0.67), number of sexual partners throughout life (P ¼ 0.6) or within the last year (P ¼ 0.78), oral contraceptive (P ¼ 0.43) or condom (P ¼ 0.37) use, and multiparity (P ¼ 0.26) were not associated with HPV infection in this study (Table II), nor were the last examination for the prevention of cervical cancer (P ¼ 0.36), the presence of genital problems (P ¼ 0.82), or a family history of cervical cancer (P ¼ 0.31; Table III).

Papillomavirus in Prison in the Amazon

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TABLE I. Distribution of Women in the Study According to the Results of Molecular Biology Tests. Ananindeua/PA, 2010 Variable

Category

n˚ Women

% Women

PCR (HPV)

Positive Negative Positive Negative Positive

8 182 15 175 20

4.2 95.8 7.9 92.1 10.5

Negative

170 190

89.5 100.0

NESTED PCR (HPV) PCR or NESTED PCR (HPV)

were identified in women with low-grade squamous intraepithelial lesions (Table III). On the other hand, high-grade squamous intraepithelial lesions, which comprised grade II and III cervical intraepithelial neoplasia, were observed in 1.0% (n ¼ 2) of cases and were not associated with HPV infection (Table III). No cases of invasive adenocarcinoma or squamous cell carcinoma were diagnosed in the study population. DISCUSSION

However, it was possible to infer the results of some factors that were strongly associated with HPV infection, such as the presence of grade I cervical intraepithelial neoplasia (n ¼ 33, 17.5%; P < 0.1) and lesions consistent with viral cytopathic effects associated with the presence of grade I cervical intraepithelial neoplasia (n ¼ 44, 23%; P ¼ 0.02); the latter

The presence of HPV was 10.5% (20/190) of the analyzed samples (Table I), a value that is in agreement with the findings of Franco et al. [1999] in a study of 1,425 women in the state of Sa˜o Paulo, Brazil. Worldwide, several reports indicate a high incidence of inflammatory, pre-neoplastic, or neoplastic HPV-associated cervical lesions [Nichols et al., 2013], the prevalence and incidence of which is high mainly in underdeveloped and developing countries [Mehta et al., 2013], thus confirming the importance of studies

TABLE II. Distribution of Study Subjects According to the Selected Variables. Ananindeua/PA, 2010 Variable Age range (years) 18–25 26–44 45–60 Marital status Married/stable union Single Education level >8 years 8 years Smoked in life No Yes Currently smoke Yes No First sexual intercourse (Coitarca) 15 years >15 years N˚ sexual partners 4 or more 0 or 3 N˚ sexual partners in the last year 0 or 1 2 or more Condom use sexual Never/sometimes Always Use of oral contraceptives in the life No Yes Contraceptive use currently No Yes Multiparity 0 or 3 4 or more

n

HPV

%

PR

P-value

68 103 19

8 8 4

11.8 7.8 21.1

1 0.6 2.0

0.20

70 120

11 9

15.7 7.5

2.3

0.07

38 152

5 15

13.2 9.9

1.3

0.55

38 152

5 15

13.2 9.9

1.4

0.55

105 79

11 8

10.5 10.1

1.0

0.86

139 50

16 4

11.5 8.0

1.5

0.67

124 50

15 4

12.1 8.0

1.5

0.60

136 49

14 4

10.3 8.2

1.3

0.78

152 38

18 2

11.8 5.3

2.4

0.37

75 115

10 10

13.3 8.7

1.6

0.43

174 16

19 1

10.9 6.3

1.8

0.70

126 64

16 4

12.7 6.3

2.2

0.26

PR, prevalence ratio; 95% CI, 95% confidence interval.  Fisher’s exact test (a  0.05).  Variables with % response ignored (values lower than 190).

J. Med. Virol. DOI 10.1002/jmv

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de Aguiar et al. TABLE III. Prevalence of Genital HPV Infection in Women in the Study According to Some Variables. Ananindeua/PA, 2010

Variable/category Last exam PCC 3 years or more 0 or 2 years STD No Yes Genital problems No Yes Family cervical cancer No Yes NIC I Positive Negative Viral cytopathic effect Positive Negative

HPV (%)

113 (61.5%) 71 (38.5%) 184

14 (12.5%) 5 (7%) 19

157 (85.8%) 26 (14.2%) 183

20 (12.7%) 0 (0%) 20

66 (35%) 124 (65%) 190

6 (9%) 14 (11.3%) 20

1.1

0.82

140 (85%) 26 (15%) 166

17 (12%) 1 (3.8%) 18

3.4

0.31

33 (17.5%) 157 (82.5%) 190

8 (24.2%) 12 (7.6%) 20

3.8

Human papillomavirus: prevalence and factors associated in women prisoners population from the Eastern Brazilian Amazon.

This study aimed to examine the prevalence of human papillomavirus (HPV) and the associated factors among female prisoners in Ananindeua City, State o...
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