Pap smear and colposcopy findings in female inmates of a prison unit in the state of São Paulo, Brazil

Summary

Objective: The objective of this study was to evaluate the Pap smear and colposcopy findings in female inmates in a prison unit in the state of São Paulo, Brazil. Methods: A retrospective cross-sectional study was carried out by analyzing the Pap smear and colposcopy examinations of female inmates in a prison unit. The following socio-demographic data were assessed: age, nationality, level of education, marital status, height, weight, ethnicity, occupation, religion, sexual orientation, and presence of tattoos. Results: The sample consisted of 894 women who had a Pap smear, the majority of whom were Brazilian (93.6%), 41.1% had an incomplete primary education, 58.5% were single, 50.1% were white, 60.7% had tattoos, and the predominant religion was Catholicism at 42.8%. Regarding sexual orientation, 124 (13.9%) women identified as bisexual, 640 (71.6%) as heterosexual, and 127 (14.2%) as homosexual. Most Pap smears showed benign findings (86.5%). Of the female inmates who had a Pap smear, 121 (13.5%) were referred for colposcopy. Altered colposcopy findings occurred in 95 (10.6%), with the most common findings being high-grade squamous intraepithelial lesions 36 (4.0%) and low-grade squamous intraepithelial lesions 27 (3.0%). The majority of women (96.0%) had no clinical signs of human papillomavirus – HPV (anogenital verrucous lesions) and only 36 (4.0%) had lesions suggestive of HPV on Pap smears. There were more HIV cases in the group with HPV verrucous lesions (P = 0.013). Conclusion: We observed 13.5% and 78.5% of abnormal findings in Pap smears and colposcopy, resp.), in female inmates in a prison unit in the state of São Paulo, Brazil.

Keywords:

HPV – prison – female inmates – Pap smear – colposcopy

Introduction

In mid-2023, the world’s prison population was approximately 11.7 million, and Brazil’s share was 644,305 inmates, of which 27,375 (4.25%) were women, making it the third largest in the world, behind the United States and China, which are first and second, respectively [1]. Brazil has 1,384 prison units with an official capacity of 481,835 places, an occupancy rate of 133.7%, and 27.9% of inmates are in pre-trial detention. In mid-2023, the prison population in the State of São Paulo was 195,787 (30.1%), of which 8,520 were women, representing 4.34% of the State’s prisoners and 31.12% of all women prisoners in Brazil [2].

The confinement experienced by female inmates and the consequent deprivation of contact with family members promote expectations that can result in a continuous process of physical and emotional stress, which can lead to a greater risk of physical and mental illness [3–5]. This risk can also be increased by an unbalanced diet and a sedentary lifestyle, leading to the occurrence of certain diseases, such as cardiovascular, metabolic and oncological diseases, among others [6–8]. It should also be considered that female inmates in Brazil are part of a younger population with some characteristics, such as unprotected sex and relationships with multiple partners, which may be associated with a higher risk of sexually transmitted diseases, such as human papillomavirus (HPV), which in turn is associated with a higher risk of cervical cancer [9,10].

In terms of oncologic impact, female inmates have few tests available for early detection, the most available being preventive cytology for cervical cancer (Pap smear or oncologic colpocytology) [11,12]. The conventional Pap smear is a low-cost, easy-to-use method and the gold standard for cervical cancer screening [13], which is particularly important in the prison system. Colposcopy is a procedure performed by a specialist in pathologies of the lower genital tract, usually after an abnormal Pap smear result, which can provide targeted biopsies [14]. However, the colposcope device and experienced examiners to perform the examination are usually not available in the majority of unit prisons [15].

The objective of this study was to evaluate the Pap smear and colposcopy findings in female inmates in a prison unit in the State of São Paulo, Brazil.

 

Materials and methods

A retrospective cross-sectional study was carried out between January 2015 and December 2020 by analyzing the Pap smear and colposcopy examinations of female inmates in a prison unit (Centro de Detenção Provisória – CPP do Butantan) located in the city of São Paulo, Brazil.

The study included the following socio-demographic data: age, nationality, level of education, marital status, height, weight, ethnicity, occupation, religion, sexual orientation, and presence of tattoos. We described the time interval between the last Pap smear and the time of the new one, and whether the inmates had previously had a Pap smear. In addition, the time interval between the negative Pap smear and the subsequent Pap smear, colposcopy, and clinical signs such as the presence of verrucous lesions in the anogenital region. The outcome of colposcopy and the treatment given were also included, and the co-infections present in the Pap smears.

For the conventional Pap smear examination, female inmates were referred to the outpatient medical center (Centro Assistencial Cruz de Malta) and underwent a gynecological examination in which secretions were collected from the vaginal sac with a spatula and from the cervical region of the uterus with a brush. All Pap smears were collected by a single experienced examiner (FMA). Pregnant women were excluded, as well as those who did not want to undergo the Pap smear. We used the following classification for the Pap smear:

class I: absence of abnormal or atypical cells (“normal”);

class II: cellular atypia, but no evidence of malignancy;

class III: cytology suggestive, but not conclusive of malignancy;

class IV: cytology strongly suggestive of malignancy;

class V: cytology conclusive for malignancy [16].

 

The colposcopy examinations were performed in two services (Maternidade Escola de Vila Nova Cachoeirinha e Santa Casa de Misericórdia de São Paulo) by a single experienced examiner (ABC) using the DF Vasconcelos device (Valença, Brazil). We used the following classification for the Colposcopy findings:

Squamous cell abnormalities:

1. atypical squamous cells of undetermined significance – ASC-US;

2. atypical squamous cells which cannot exclude a high-grade lesion – ASC-H;

3. low-grade squamous intraepithelial lesion – LSIL;

4. high-grade squamous intraepithelial lesion – HSIL;

5. squamous cell carcinoma.

 

Abnormalities of glandular cells:

1. atypical glandular cells;

2. adenocarcinoma in situ;

3. adenocarcinoma (endocervical, endometrial, extrauterine) [17].

 

Data were transferred to an Excel spreadsheet (Microsoft Corp., Redmond, WA, USA) and statistical analyses were performed using IBM SPSS Statistics version 24 (IBM Corp., Armonk, NY, USA) and R software version 3.6.3. Statistical analysis was performed using summary measurements such as mean, median, Min. and Max. values, standard deviation, absolute and relative frequencies (percentages), as well as pie charts, bar graphs, box plots, and one-dimensional scatter plots. The inferential analyses used to confirm or refute the evidence found in the descriptive analysis were Mann-Whitney, Pearson’s chi-square, and Fisher’s exact or its extension. A 5% alpha significance level was used for all inferential conclusions.

Results

The sample selected for this study consisted of 894 female inmates who had a Pap smear, the majority of whom were Brazilian (93.6%), followed by South Africans (0.9%) and Bolivians (0.9%). The mean age of these women was 34.9 years, ranging from 19 to 73 years. The mean body mass index (BMI) was 25.1 kg/m², ranging from 15.1 to 49.6 kg/m².

Tab. 1 shows the socio-demographic characteristics: 367 (41.1%) of women had an incomplete primary education, 523 (58.5%) were single, 448 (50.1%) were white, 543 (60.7%) had tattoos, and the predominant religion was Catholicism (42.8%) and Evangelical (42.1%). Regarding sexual orientation, 124 (13.9%) women identified as bisexual, 640 (71.6%) as heterosexual, and 127 (14.2%) as homosexual. In terms of occupation, the majority were housewives (24.3%), followed by domestic workers (11.2%), shopkeepers (3.4%), and hairdressers (3.1%).

Regarding Pap smears, 285 (31.9%) had them less than 3 years ago, 467 (52.2%) had them 3 years ago or more, and 58 (6.5%) reported never having them. Most Pap smears showed benign findings (86.5%). Altered colposcopy findings occurred in 95 (10.6%) women, with the most common findings being HSIL (36, 4.0%) and LSIL (27, 3.0%). The majority of women (96.0%) had no clinical signs of HPV (presence of anogenital verrucous lesions) and only 36 (4.0%) women had lesions suggestive of HPV on Pap smears. Regarding the outcomes, the majority had clinical follow-up (81,2 90.8%), followed by extended biopsy (43, 4.8%) (Tab. 2). We observed co-infections in 181 (20.2%) Pap smear results, with the main agents being Gardnerella vaginalis/Mobiluncus sp. (65.2%), Trichomonas vaginalis (28.7%), and Candida sp. (6.1%).

Tab. 3 shows the distribution of alterations in the Pap smear according to socio-demographic characteristics of female inmates. We observed a higher number of homosexuals in the LSIL group (P < 0.001), a shorter time until colposcopy in the ASC-US group (P = 0.025), a higher number of HPV verrucous lesions in the LSIL group (P < 0.001), and a higher number of HIV in the LSIL group (P < 0.001).

Of the female inmates who had a Pap smear, 121 (13.5%) were referred for colposcopy. Tab. 4 shows the distribution of alterations in colposcopy according to socio-demographic characteristics of female inmates. The HSIL group was older (P = 0.033), the cancer group had more bisexuals (P = 0.005), and a longer time until colposcopy (P < 0.001).

Tab. 5 shows the relationships between HPV verrucous lesions and socio-demographic characteristics of female inmates. There were more benign findings in the group without HPV verrucous lesions and LSIL group with HPV verrucous lesions (P < 0.001). There was more clinical follow-up in the group without HPV verrucous lesions and extended biopsy in the group with HPV verrucous lesions (P < 0.001). There were more HIV cases in the group with HPV verrucous lesions (P = 0.013).

 

 

Discussion

In terms of sociodemographic characteristics, the majority of all samples were Brazilian, with incomplete primary education, single, white, and Catholic. In a study developed by Silva et al. [18] with 352 women in prisons of Mato Grosso do Sul, Midwest of Brazil, the majority was Brazilian, with incomplete primary education and mixed race. The differences between the ethnicities of both studies are probably a consequence of the different racial distributions between both Brazilian states [19]. In a broader study involving 15 female prisons in eight states of all Brazilian regions with a sample of 1,327 women, 65.1% were black or mixed race, with incomplete primary education, single, and Catholic [20].

We also assessed other socio-demographic characteristics such as sexual orientation and occupation. Of these women, 13.9% identified as bisexual, 71.6% as heterosexual, and 14.2% as homosexual. Farel et al. [21] conducted qualitative interviews with 29 African--American women in prison (15 HIV positive, 14 HIV negative). Women reported complex sexual risk profiles during the 6 months before incarceration, including sex with women as well as prior sexual partnerships with both men and women. In a Brazilian study on the sexual behavior of 18 women prisoners, 33.3% reported health behaviors such as sexually transmitted infections, 27.7% related to the use of male condoms, 16.6% prevented unwanted pregnancies, and 11.1% followed good health care and hygiene practices [22]. Regarding occupation, the majority were housewives, followed by domestic workers. In a study by de Araujo et al. [20], the majority of women prisoners were domestic workers (31.8%).

Regarding Pap smears, 86.5% of the exams showed benign findings. We observed a higher number of homosexuals in the LSIL group, a shorter time until colposcopy in the ASC-US group, a higher number of HPV warty lesions in the LSIL group, and a higher number of HIV cases in the LSIL group. Audi et al. [23] performed a study with 702 female inmates aged between 25 and 64 years and in a unit prison in the São Paulo state for not less than 12 months. The mean women’s age was 34.7 years and the performance of Pap smear was 26.3%. There were no differences in prevalence when assorted by age group, marital status, ethnicity/race, religion, education, income, work at the prison, and the fact of having children. Silva et al. [18] found that of the incarcerated women who had received a Pap smear, 298 (69.8%) reported no cellular changes at the time, while 70 (16.4%) reported changes, of which 42 (60.0%) reported infection as the most common change. Delage de Luget et al. [24] estimated the prevalence of cervical dysplasia among incarcerated women in a prison unit in Marseille, France. A total of 201 Pap smears were evaluated, 135 were normal (67.2%), 33 were unsatisfactory (16.4%), and 33 (16.4%) were abnormal.

We observed 20.2% of co-infections in Pap smears results, including Gardnerella vaginalis/Mobiluncus sp. (65.2%), Trichomonas vaginalis (28.7%), and Candida sp. (6.1%). A Brazilian study assessed the sexual behavior of partners of female inmates, being that 41.2% of them reported a history of sexually transmitted diseases. Association was observed between having more than one partner in the last 12 months, sexual violence, having sex for money, and under the influence of alcohol and drugs [25]. In a study of 387 incarcerated women from the Rhode Island Department of Corrections who submitted a self-collected vaginal swab for APTIMA transcription-mediated amplification testing, the prevalence of Trichomonas vaginalis was 14% [26]. In a study of juvenile incarcerated women in Kingston, Ontario, Canada, of the women tested, 4% were positive for Neisseria gonorrhoeae, 10% for Chlamydia trachomatis, 32% for bacterial vaginosis, and 5% for Trichomonas vaginalis [27].

Of the female inmates who had a Pap smear, 13.5% were referred for colposcopy and the main findings in the pathology were as follows: cancer 1.9%, chronic cervicitis 1.7%, HSIL 4.0%, and LSIL 3.0%. Downley et al. [28] evaluated 206 incarcerated women who had colposcopy. The prevalence of low-grade disease – cervical intraepithelial neoplasia grade (CIN) grade I was 406 (8.0%), while the prevalence of high-grade disease – CIN grades II and III was 250 (4.9%). Invasive squamous carcinoma occurred in 18 (0.4%) cases. Invasive cervical squamous cell carcinoma has as a main etiologic factor, infection by HPV, which presents at a high prevalence in incarcerated women [29]. In Brazil, excluding non-melanoma skin tumors, cervical cancer is the third most common type of cancer among women. For each year of the three-year period 2023–2025, 17,010 new cases were estimated, which represents a crude incidence rate of 15.38 cases per 100,000 women [30].

The strengths of our study were the large sample size of Pap smears, and the fact that both Pap smears and colposcopy were performed by only two experienced examiners, which could increase sensitivity of methods.

In summary, we presented the Pap smear and colposcopy findings of female inmates of a prison unit in São Paulo State, Brazil. We observed 13.5% and 78.5% of abnormal findings in the Pap smear and colposcopy, respectively. These findings can contribute to the development of public policies aimed at improving the health care of female inmates.