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Profile of women with cervical changes from a city in the Northeast Brazil

ABSTRACT

Introduction:

In Brazil, cervical cancer is the fourth leading cause of cancer death. It reached 5,430 deaths in the year 2013, with estimated 16,370 new cases by 2018. Its occurrence has been associated with previous human papillomavirus (HPV) infection for the development of intraepithelial lesions; however, several factors can influence this appearance, including number of sexual partners and infections by other microorganisms.

Objective:

The profile of women from the city of Caruaru, Pernambuco, Brazil, with atypia, cervical intraepithelial lesions and cancer, was verified.

Material and method:

Documentary, analytical, retrospective study, carried out through the collection of information in the database of the State Department of Health of Pernambuco, by TabNet, referring to the tests in the laboratory of the municipality of Caruaru, Pernambuco, Brazil.

Results:

During the study period, 18,466 tests were evaluated. From the samples evaluated, 735 (4.31%) were squamous and glandular atypia, 167 (0.98%) intraepithelial lesions, and one (0.005%) cancer. Coccus, Gardnerella vaginalis and Lactobacilli were the most evident agents in cervical alterations.

Discussion:

Studies demonstrate the intimate relationship between infectious agents and the development of cervical lesions and cancers. Gardnerella vaginalis was the most frequent agent in the presence of abnormalities was identified as a facilitator of HPV penetration.

Conclusion:

Women infected by Gardnerella vaginalis and older than 30 years of age are more exposed to the development of alterations. Guidelines on prevention and screening should be continuous strategies in public services. Understanding these risk factors is a paramount concern because they are involved in the prevention and etiology process of cervical lesions and cancer.

Key words:
risk factors; carcinoma of the uterine cervix; sexually transmitted diseases; papillomavirus infections

RESUMEN

Introducción:

En Brasil, el cáncer de cuello de útero es la cuarta causa de muertepor cáncer, con 5.430 muertes en 2013 y previsión de 16.370 nuevos casos para 2018. Su aparición se asocia a la infección previa por el virus delpapiloma humano (VPH) para el desarrollo de lesiones intraepiteliales; no obstante, diversos factores pueden influenciarle, por ejemplo, número de companeros sexuales e infeccionespor otros microrganismos.

Objetivo:

Se ha comprobado el perfil de mujeres del municipio de Caruaru, Pernambuco, Brasil, que tenían atipias, lesiones intraepiteliales cervicales y cáncer.

Material y método:

Investigación documental, analítica, retrospectiva, realizada mediante una encuesta en la base de datos del departamento de salud de Pernambuco, a través de TabNet, relativas a los exámenes en el laboratorio del municipio de Caruaru, Pernambuco, Brasil.

Resultados:

En el período del análisis, 18.466 exámenes han sido evaluados. De las muestras analizadas, 735 (4,31%) han sido de atipias escamosas y glandulares; 167 (0,98%) de lesiones intraepiteliales; y una (0,005%) de cáncer. Cocos, Gardnerella vaginalis y lactobacilos han sido los agentes más evidentes en las alteraciones cervicales.

Discusión:

Investigaciones comprueban una relación directa entre agentes infecciosos y el desarrollo de lesiones y cáncer cervical. Gardnerella vaginalis ha sido aquel más frecuente en presencia de anormalidades, pues facilita la invasión por el VPH.

Conclusión:

Mujeres mayores de 30 anos infectadas por Gardnerella vaginalis representan una exposición importante al desarrollo de alteraciones. Recomendaciones de prevención y tamizaje deben ser estrategias constantes en el serviciopúblico. Conocer estos factores de riesgo es crucial, porque ellos envuelven el proceso de prevención y etiología de las lesiones y del cáncer de cérvix.

Palabras clave:
factores de riesgo; neoplasias de cuello de útero; enfermedades de transmisión sexual; infecciones por virus del papiloma humano

RESUMO

Introdução:

No Brasil, o câncer do colo do útero é a quarta causa de morte por câncer. Atingiu 5.430 mortes no ano de 2013, com estimativa de 16.370 novos casos para 2018. Sua ocorrência tem sido associada à infecção prévia pelo papilomavírus humano (HPV) para o desenvolvimento de lesões intraepiteliais, no entanto, vários fatores podem influenciar esse aparecimento, por exemplo, número de parceiros sexuais e infecções por outros microrganismos.

Objetivo:

Verificou-se o perfil das mulheres do município de Caruaru, Pernambuco, Brasil, com atipias, lesões intraepiteliais cervicais e câncer.

Material e método:

Estudo documental, analítico, retrospectivo, realizado por meio do levantamento de informações no banco de dados da Secretaria Estadual de Saúde de Pernambuco, pelo TabNet, referentes aos exames no laboratório do município de Caruaru, Pernambuco, Brasil.

Resultados:

No período do estudo foram avaliados 18.466exames. Das amostras avaliadas, 735 (4,31%) foram atipias escamosas e glandulares; 167 (0,98%), lesões intraepiteliais; e uma (0,005%), câncer. Cocos, Gardnerella vaginalis e lactobacilos foram os agentes mais evidentes nas alterações cervicais.

Discussão:

Estudos comprovam relação íntima dos agentes infecciosos com o desenvolvimento de lesões e cânceres cervicais. Gardnerella vaginalisfoi o agente mais frequente na presença de anormalidades, sendo identificada como facilitadora da penetração do HPV.

Conclusão:

Mulheres infectadas por Gardnerella vaginalis com idade acima de 30 anos representam maior exposição ao desenvolvimento de alterações. Orientações quanto à prevenção e ao rastreamento devem ser estratégias constantes nos serviços públicos. Entender esses fatores de risco é primordial, porque eles envolvem o processo de prevenção e etiologia das lesões e do câncer cervical.

Unitermos:
fatores de risco; neoplasias do colo do útero; doenças sexualmente transmissíveis; infecções por papilomavírus

INTRODUCTION

Cervical cancer is the third most frequent tumor among women, preceded by breast and colorectal cancer; it is the fourth leading cause of cancer death in Brazil. Cervical cancer reached 5,430 deaths in the year 2013, and for the year 2018, it presents an estimate of 16,370 new cases(11 INCA. Instituto Nacional do Câncer. Estimativa 2018, incidência de câncer no Brasil [Internet]. Available at: http://www.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp. [Acessed on: 2018, Jul 22].
http://www.inca.gov.br/estimativa/2018/s...
).

The occurrence of cervical cancer has been associated with previous human papillomavirus (HPV) infection. However, there are co-factors that may enhance the risk of developing this cancer, such as early age at sexual initiation, multiplicity of sexual partners, smoking, prolonged use of birth control pills and a history of sexually transmitted diseases (STD) - co-infections with the human immunodeficiency virus (HIV) and Trichomonas vaginalis infection(22 INCA. Instituto Nacional do Câncer. Controle do câncer do colo do útero [Internet]. Available at: http://www2.inca.gov.br/wps/wcm/connect/acoes_programas/site/home/nobrasil/programa_nacional_controle_cancer_colo_utero/deteccao_precoce. [Acessed on: 2014, Nov 11].
http://www2.inca.gov.br/wps/wcm/connect/...
) -, as well as co-infection with causative agents of bacterial vaginosis (BV), characterized by the inversion of the microbiota, with substitution of Lactobacillus sp. by the growth of anaerobic bacteria, including Gardnerella vaginalis, Atopobium vaginae and species of Mobiluncus and Prevotella spp. Several studies have observed association of BV with HPV, showing that the prevalence of this combination can reach up to 32%(33 Gillet E, Meys JF, Verstraelen H, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011; 11: 1-10.). There is a greater complexity in the types of vaginal microbiota from HPV-positive women compared with HPV-negative women(44 Gao W, Weng J, Gao Y, Chen X. Comparison of the vaginal microbiota diversity of women with and without human papillomavirus infection: a cross-sectional study. BMC Infect Dis. 2013; 13: 271-80.).

Considering microorganisms as causal factors of STD, it is essential to understand that microorganism entry may occur during sexual intercourse through the pudendal cleft, anatomical region of the female genital system(55 Linhares IM, Giraldo PC, Baracat EC. Novos conhecimentos sobre a flora bacteriana vaginal. Ver Assoc Med Bras. 2010; 56(3): 370-4.) that presents a broad and variable microbiota throughout the woman’s lifetime(66 Katz VL, Lentz G, Lobo RA, Gershenson D. Comprehensive gynecology. 5th ed. Philadelphia: Mosby/Elsevier; 2007.). However, several factors can influence the incidence of infections, such as socioeconomic status, age, sexual activity, number of sexual partners, menstrual cycle phase, and infections by other microorganisms(77 Van Belkum A, Van Der Schee C, Van Der Meijden WI, Verbrugh HA, Sluiters HJF A clinical study on the association of Trichomonas vaginalis and Micoplasma hominis infections in women attending a sexually transmited disease (STD) outpatient clinic. FEMS Immunol Med Microbiol. 2001; 32: 27-32.).

OBJECTIYE

To verify the profile of women with cervical abnormalities in the cytopathological tests performed at the municipality of Caruaru, Pernambuco, Brazil.

MATERIAL AND METHOD

This is a documentary, analytical and retrospective study that was carried out through the collection of information obtained from the database of the State Department of Health of Pernambuco [Secretaria Estadual de Saúde de Pernambuco (SESPE)]/TabNet available online.

This work was previously approved by the Research Ethics Committee of the Asces-Unita, under no. CAAE: 44804115.5.0000.5203.

The data collection was carried out from January to March 2015, involving tests carried out in the year 2013 obtained from the database of the SESPE website (http://portal.saude.pe.gov.br/), where they are in the public domain and freely accessible, in the field “Informações em Saúde” (Health Information), which has the data from the Information System of Cervical Cancer [Sistemas de Informação do Câncer do Colo do Útero (SISCOLO)], a computerized data input system developed by DATASUS in partnership with the Brazilian National Cancer Institute [Instituto Nacional do Câncer (INCA)], which collects and processes information on patient identification and cytopathological and histopathological reports, providing data for the external monitoring of the quality of the tests and directing the state managers of the programme on quality for the laboratories responsible for reading the tests in the municipality(88 DATASUS. Informações em Saúde - Sistemas - SISCOLO/SISMAMA [Internet]. Available at: http://datasus.saude.gov.br/sistemas-e-aplicativos/epidemiologicos/siscolo-sismama. [Acessed on: 2016, Feb 22].
http://datasus.saude.gov.br/sistemas-e-a...
).

Results recorded in the system with incorrect identifications, incomplete data (age, last examination, collected material) and results considered unsatisfactory for evaluation (smears obscured by inflammatory exudate, red blood cells, desiccation in more than 75% of the sample, acellular or hypocellular smears with less than 10% of the sample), were excluded from the research.

Statistical analysis was performed using the PRISM software version 6.0. The chi-square test of association was used, considering significance levelp < 0.05.

RESULTS

During the study period, the results of 18,466 cervical cytopathological tests were evaluated, of which 1,434 tests were considered unsatisfactory and were excluded from the study. Among the included samples, 735 (4.31%) were positive for squamous and glandular atypia; 167 (0.98%) for intraepithelial lesions; one (0.005%) for squamous cell carcinoma; and one (0.005%) for in situ adenocarcinoma (Table 1).

Table 1
Frequency of cervical changes in the cytopathological exams of women from the municipality of Caruaru, Pernambuco, in the year 2013

Regarding the age of the patients, they were divided into two groups: under 30 years of age, corresponding to 5,297 women (31.1%), and older than 30 years of age, totaling 11,735 (68.89%). Among the positive exams, patients under the age of 30 years resulted in a total of 337 women (37.27%), while 567 (62.72%) represented those aged older than 30 years.

Regarding the educational level, 610 (3.58%) reported to be illiterate; 3,075 (18.05%) had incomplete elementary education; 1,138 (6.68%), complete elementary education; 1,224 (7.18%), complete high school education; 171 (1%), complete higher school education; and 10,814 (63.49%) presented the schooling field unfilled/ignored. Among the positive exams, 34 (3.76%) were illiterate; 140 (15.48%) had incomplete elementary education; 71 (7.85%), complete elementary education; 64 (7.07%), complete high school education; only six (0.66%) had complete higher school education and 589 (65.15%) presented the schooling field unfilled/ignored.

Regarding the periodicity of the examination, the majority affirmed that they had already taken the test, totaling 14,811 (86.96%); 2,221 (13.04%) stated that they did not have being through it, did not know or did not remember having taking the test previously. Among the tests considered positive, 134 (14.82%) did not have, did not remember or did not know if they had previously taken the test, and 770 (85.18%) said that they had already taken the test (Table 2).

Table 2
Profile of women with cervical changes from the municipality of Caruaru, Pernambuco, 2013

DISCUSSION

The persistence of infectious agents is closely linked to the induction of carcinogenesis. In cases where infections are quickly disposed by the immune system, pathological abnormalities are usually not observed, whereas in chronic infections, the risk of developing cancer increases considerably. The literature demonstrates that specific viruses associated with cancer, such as high-risk HPV in the mucous membranes, the persistence of its infection causes damage to deoxyribonucleic acid (DNA), which can trigger the activation of cellular oncogenes or the inactivation of tumor suppressors genes, contributing to the neoplastic transformation of the infected cells(99 IARC. International Agency for Research on Cancer [Internet]. Available at: http://www.iarc.fr/&prev=search. [Acessed on: 2014, Oct 29].
http://www.iarc.fr/&prev=search...
). The oncogenic subtypes of HPV 16 and 18 are responsible for the origin of about 70% of cases of invasive cervical cancer. Together with the aspects related to HPV infection, the following are considered risk factors for the development of this disease: early sexual initiation, multiplicity of sexual partners, smoking, simultaneous infection with infectious agents such as early age at sexual initiation, multiplicity of sexual partners, smoking, presence of co-infections of infectious agents, such as the human immunodeficiency virus (HIV) andChlamydia trachomatis, use of birth control pills, multiple births and low intake of vitamin(1010 INCA. Instituto Nacional do Câncer/Ministério da Saúde. Nomenclatura brasileira para laudos cervicais e condutas preconizadas: recomendações para profissionais de saúde. J Bras Patol Clin Med Lab. 2006. 2006; 42(5): 351-73.,1111 Munoz N, Bosch FX, de Sanjose S, et al; International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003; 348(6): 518-27.). Age is intimately associated with the risk of developing any neoplasia throughout life(1212 Gomes CHR, Nobre AL, Aguiar GN, et al. Avaliação do conhecimento sobre detecção precoce do câncer das estudantes de medicina de uma universidade pública. Rev Bras Cancerol. 2008; 54(1): 25-30.).

The lack of prevention programs is another important factor, because by performing the cytopathological test, it is possible to detect the precursor lesion of cervical cancer until fifteen years before the manifestation of the disease. This test is easy to implement, inexpensive and effective(1313 Ramos SP Exame ginecológico preventivo do câncer Papanicolaou: citologia oncótica [Internet]. Available at: http://www.gineco.com.br/saude-feminina/doencas-femininas/cancer-do-colo-do-utero. [Acessed on: 2014, Oct 11].
http://www.gineco.com.br/saude-feminina/...
).

Cervical cancer is also related to a number of epidemiological factors that can be minimized through prevention and the efficient performance of health professionals in an organized way. Another important topic is the women compliance to cytopathological test, which is decisive for the incidence of this neoplasm(1414 Smeltzer SC, Bare BG. Tratado de enfermagem médico-cirúrgico. 9 ed. Rio de Janeiro: Guanabara Koogan; 2002.).

In the present study, Gardnerella vaginalis was the most frequent agent in the presence of abnormalities. Studies have shown that this bacterium is identified as facilitating the penetration of HPV due to its aggression to tissue, thus increasing the risk of developing cervical cancer(1515 Murta EFC, Souza MAH, Adad SJ, et al. Persistência da infecção por papilomavírus humano: análise da idade, sexo, raça, cor, hábito de fumar e método contraceptivo. J Bras Ginecol. 1998; 108: 117-20.). However, in the present study, the significant presence of this bacterium in the appearance of lesions was brought to light, corroborating the other studies(33 Gillet E, Meys JF, Verstraelen H, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011; 11: 1-10.,44 Gao W, Weng J, Gao Y, Chen X. Comparison of the vaginal microbiota diversity of women with and without human papillomavirus infection: a cross-sectional study. BMC Infect Dis. 2013; 13: 271-80.,1616 Rodriguez-Cerdeira C, Sanchez-Blanco E, Alba A. Evaluation of association between vaginal infections and high-risk human papillomavirus types in female sex workers in Spain. SRN Obstet Gynecol. 2012; 1: 1-7.).

VB can favor HPV infection due to its polymicrobial etiology, which spreads its exotoxins by adhering to the mucosal surfaces, thereby attacking it(1717 Sexually transmitted diseases treatment guidelines 2002. Centers for Diseases Control and Prevention. MMWR Recomm Rep. 2002; 51(RR-6): 1-78.). Effective treatment of this VB condition is essential for the reduction of penetration and exposure to HPV.

It was highlighted that one of the important factors is age, therefore, having as parameters some studies(1818 Nai GA, Mello ALP, Ferreira AD, Barbosa RL. Frequência de Gardnerella vaginalis em esfregaços vaginais de pacientes histerectomizadas. Rev Assoc Med Bras. 2007; 52(2): 162-5.

19 Andriolo A. Guias de medicina ambulatorial e hospitalar. São Paulo: Editora Manole; 2005.
-2020 Schechter M, Marangoni DV. Doenças infecciosas: conduta, diagnóstico e terapêutica. 2 ed. Rio de Janeiro: Guanabara Koogan; 1998.), two age groups were used: up to 29 years of age and older or equal to 30 years of age. According to the data analyzed, 5,297 patients were younger than 30 years of age, of whom 337 presented positive cytology, p =0.0001 and relative risk (RR) 1,317; 11,735 patients were aged > 30 years, of which 567 presented positive cytology, p = 0.0001 and RR 0.7595. The significance of the data is clear in relation to the ages presented, but the group > 30 years presented a higher frequency in the development of cervical abnormalities.

In the study by Silva et al. (2014)(2121 Silva DSM, Silva AMN, Brito LMO, Gomes SRL, Nascimento MDSB, Chein MBC. Rastreamento do câncer do colo do útero no estado do Maranhão, Brasil. Ciência & Saúde Coletiva. 2014; 19(4): 1163-70.), unfilled schooling corresponded to 89.6%. Considering the importance of schooling in combating transmission of HPV, 10,814 patients with unknown schooling were observed, of which 589 presented positive cytology. These data corroborate an associated risk. In the present study, it was observed that the percentage of women with incomplete elementary education corresponded to 18.05%, followed by those with complete elementary 6.68%, high school 7.18% and higher school education 1%. In the study by Thuler et al. (2012)(2222 Thuler LCS, Bergmann A, Casado L. Perfil das pacientes com câncer do colo do útero no Brasil, 2000-2009: estudo de base secundária. Rev Bras Cancerol. 2012; 58(3): 351-7.), which evaluated cancer patients, the low schooling (incomplete elementary school or less) corresponded to 70%. The schooling variable was shown to be low, although most of the exams presented this item as ignored/unfilled, corresponding to 63.48% among the performed examinations considered satisfactory.

Regarding the periodicity of cytopathological test performance, in the study by Silva et al. (2014)(2121 Silva DSM, Silva AMN, Brito LMO, Gomes SRL, Nascimento MDSB, Chein MBC. Rastreamento do câncer do colo do útero no estado do Maranhão, Brasil. Ciência & Saúde Coletiva. 2014; 19(4): 1163-70.), most women (92%) who presented altered results had also performed the test in the previous year, data similar to those of the present study, which showed that 85.2% of these women were tested in the previous year. However, a higher percentage of atypical squamous cells of undetermined significance (ASC-US) and atypical squamous cells-cannot exclude high-grade squamous intraepithelial lesions (ASC-H), and may or may not be associated with incipient lesions. Despite the low educational level of the patients, the majority with altered tests recognizes the importance of the scrutiny program.

CONCLUSION

The presence of cocci bacteria and supracytoplasmic bacilli suggestive of Gardnerella vaginalis was found in most of the tests with cytological abnormalities. It is important to consider that women older than 30 years of age infected by Gardnerella vaginalis should be monitored by cervical cytopathology tests. Even with the low level of education among patients with altered tests, it is worth considering the existence of effective awareness on the relevance of cervical cancer screening. Thus, guidelines related to the prevention of cervical cancer should be a continuous strategy in the public health services, contributing to an effective cervical cancer screening.

REFERENCES

  • 1
    INCA. Instituto Nacional do Câncer. Estimativa 2018, incidência de câncer no Brasil [Internet]. Available at: http://www.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp [Acessed on: 2018, Jul 22].
    » http://www.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp
  • 2
    INCA. Instituto Nacional do Câncer. Controle do câncer do colo do útero [Internet]. Available at: http://www2.inca.gov.br/wps/wcm/connect/acoes_programas/site/home/nobrasil/programa_nacional_controle_cancer_colo_utero/deteccao_precoce [Acessed on: 2014, Nov 11].
    » http://www2.inca.gov.br/wps/wcm/connect/acoes_programas/site/home/nobrasil/programa_nacional_controle_cancer_colo_utero/deteccao_precoce
  • 3
    Gillet E, Meys JF, Verstraelen H, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011; 11: 1-10.
  • 4
    Gao W, Weng J, Gao Y, Chen X. Comparison of the vaginal microbiota diversity of women with and without human papillomavirus infection: a cross-sectional study. BMC Infect Dis. 2013; 13: 271-80.
  • 5
    Linhares IM, Giraldo PC, Baracat EC. Novos conhecimentos sobre a flora bacteriana vaginal. Ver Assoc Med Bras. 2010; 56(3): 370-4.
  • 6
    Katz VL, Lentz G, Lobo RA, Gershenson D. Comprehensive gynecology. 5th ed. Philadelphia: Mosby/Elsevier; 2007.
  • 7
    Van Belkum A, Van Der Schee C, Van Der Meijden WI, Verbrugh HA, Sluiters HJF A clinical study on the association of Trichomonas vaginalis and Micoplasma hominis infections in women attending a sexually transmited disease (STD) outpatient clinic. FEMS Immunol Med Microbiol. 2001; 32: 27-32.
  • 8
    DATASUS. Informações em Saúde - Sistemas - SISCOLO/SISMAMA [Internet]. Available at: http://datasus.saude.gov.br/sistemas-e-aplicativos/epidemiologicos/siscolo-sismama [Acessed on: 2016, Feb 22].
    » http://datasus.saude.gov.br/sistemas-e-aplicativos/epidemiologicos/siscolo-sismama
  • 9
    IARC. International Agency for Research on Cancer [Internet]. Available at: http://www.iarc.fr/&prev=search [Acessed on: 2014, Oct 29].
    » http://www.iarc.fr/&prev=search
  • 10
    INCA. Instituto Nacional do Câncer/Ministério da Saúde. Nomenclatura brasileira para laudos cervicais e condutas preconizadas: recomendações para profissionais de saúde. J Bras Patol Clin Med Lab. 2006. 2006; 42(5): 351-73.
  • 11
    Munoz N, Bosch FX, de Sanjose S, et al; International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003; 348(6): 518-27.
  • 12
    Gomes CHR, Nobre AL, Aguiar GN, et al. Avaliação do conhecimento sobre detecção precoce do câncer das estudantes de medicina de uma universidade pública. Rev Bras Cancerol. 2008; 54(1): 25-30.
  • 13
    Ramos SP Exame ginecológico preventivo do câncer Papanicolaou: citologia oncótica [Internet]. Available at: http://www.gineco.com.br/saude-feminina/doencas-femininas/cancer-do-colo-do-utero [Acessed on: 2014, Oct 11].
    » http://www.gineco.com.br/saude-feminina/doencas-femininas/cancer-do-colo-do-utero
  • 14
    Smeltzer SC, Bare BG. Tratado de enfermagem médico-cirúrgico. 9 ed. Rio de Janeiro: Guanabara Koogan; 2002.
  • 15
    Murta EFC, Souza MAH, Adad SJ, et al. Persistência da infecção por papilomavírus humano: análise da idade, sexo, raça, cor, hábito de fumar e método contraceptivo. J Bras Ginecol. 1998; 108: 117-20.
  • 16
    Rodriguez-Cerdeira C, Sanchez-Blanco E, Alba A. Evaluation of association between vaginal infections and high-risk human papillomavirus types in female sex workers in Spain. SRN Obstet Gynecol. 2012; 1: 1-7.
  • 17
    Sexually transmitted diseases treatment guidelines 2002. Centers for Diseases Control and Prevention. MMWR Recomm Rep. 2002; 51(RR-6): 1-78.
  • 18
    Nai GA, Mello ALP, Ferreira AD, Barbosa RL. Frequência de Gardnerella vaginalis em esfregaços vaginais de pacientes histerectomizadas. Rev Assoc Med Bras. 2007; 52(2): 162-5.
  • 19
    Andriolo A. Guias de medicina ambulatorial e hospitalar. São Paulo: Editora Manole; 2005.
  • 20
    Schechter M, Marangoni DV. Doenças infecciosas: conduta, diagnóstico e terapêutica. 2 ed. Rio de Janeiro: Guanabara Koogan; 1998.
  • 21
    Silva DSM, Silva AMN, Brito LMO, Gomes SRL, Nascimento MDSB, Chein MBC. Rastreamento do câncer do colo do útero no estado do Maranhão, Brasil. Ciência & Saúde Coletiva. 2014; 19(4): 1163-70.
  • 22
    Thuler LCS, Bergmann A, Casado L. Perfil das pacientes com câncer do colo do útero no Brasil, 2000-2009: estudo de base secundária. Rev Bras Cancerol. 2012; 58(3): 351-7.

Publication Dates

  • Publication in this collection
    09 May 2019
  • Date of issue
    Jan-Feb 2019

History

  • Received
    29 Aug 2016
  • Reviewed
    27 Aug 2018
  • Accepted
    30 Nov 2018
  • Published
    20 Feb 2019
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