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Article

High Burden of Chlamydia trachomatis and Human Papillomavirus Infections in Low-Income Female University Students from Public Schools in the Brazilian Amazon

by
Leonardo Miranda dos Santos
1,2,*,†,
Rodrigo Covre Vieira
1,†,
Louise de Souza Canto Covre
1,
Milena Cristina Martins da Silva
1,
Thiago de Matos Bezerra
1,
Geraldo Mariano Moraes de Macedo
3,
Edna Aoba Yassui Ishikawa
1,
Karla Valéria Batista Lima
4,
Maísa Silva de Sousa
1 and
Rodrigo Vellasco Duarte Silvestre
5
1
Laboratory of Molecular and Cellular Biology, Center for Tropical Medicine, Federal University of Para, Belem 66075-110, PA, Brazil
2
State Department of Education of Pará, Government of the State of Pará, Belem 66020-080, PA, Brazil
3
Laboratory of Tropical Dermatology, Center for Tropical Medicine, Federal University of Para, Belem 66075-110, PA, Brazil
4
Bacteriology and Mycology Section, Evandro Chagas Institute, Ananindeua 67030-000, PA, Brazil
5
Papillomavirus and Retrovirus Laboratory, Virology Section, Evandro Chagas Institute, Ananindeua 67030-000, PA, Brazil
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Microorganisms 2026, 14(6), 1176; https://doi.org/10.3390/microorganisms14061176
Submission received: 28 August 2025 / Revised: 15 October 2025 / Accepted: 4 November 2025 / Published: 23 May 2026
(This article belongs to the Special Issue Chlamydiae and Chlamydia-Like Infections)

Abstract

Sexually transmitted infections (STIs) caused by C. trachomatis and HPV are the most prevalent worldwide. College students are characterized by being young women of reproductive age who may have risky sexual behavior. To describe the prevalence and factors associated with endocervical infection by C. trachomatis and HPV in college women in the Brazilian Amazon. Endocervical secretions were collected. The ompA gene of C. trachomatis and the L1 gene of HPV were detected. The Chi-square test, Fisher’s exact test, G test, Odds Ratio, and Multiple Logistic Regression were used with 95% confidence interval and p ≤ 0.05. The overall prevalence of endocervical infection by C. trachomatis was 8.3% (25/302) and by HPV was 28.9% (87/302). Low income was associated with sexually transmitted infection by C. trachomatis (14.8%, p = 0.0336). Those under 25 years old had twice the chance of HPV infection [39.3%, (OR: 2.6989), 95% CI: 1.6054–4.5371, p = 0.0002], as did women without children [31.8%, (OR: 2.333), CI: 1.1235–4.8461, p = 0.0307]. Women who did not study in a public school had 63% reduced risk of acquiring HPV infection [45.8% (OR: 0.3713), CI: 0.1951–0.7064, p = 0.0035]. C. trachomatis and HPV infections were present in low-income, childless young women who attended public schools, requiring the intensification of STI prevention policies in the Amazon region.

1. Introduction

Sexually transmitted infections (STIs) caused by Chlamydia trachomatis and human papillomavirus are serious global health issues, as they are prevalent infections with widespread exposures levels in the world’s population, becoming a challenge for screening schemes, with 128.5 million annual cases of C. trachomatis and a global prevalence of 31% for HPV [1,2]. Endocervical infection by C. trachomatis increases the persistence of HPV infection and its genetic materials may be present in 99% of cervical cancers [3,4], in addition to facilitating HIV infection [5].
C. trachomatis is an obligate intracellular bacterium classified into 19 genotypes according to the variability profile in its ompA gene, with genotypes A to C causing trachoma, genotypes L1 to L3 causing lymphogranuloma venereum, and genotypes D to K causing endocervical infection that is asymptomatic in up to 80% of women [6]. Infections by C. trachomatis can progress in up to 19.7% of cases to Pelvic Inflammatory Disease (PID) and subsequent permanent damage, such as infertility and ectopic pregnancies [7,8,9]. HPV is a non-enveloped virus of the Papillomaviridae family that infects the skin and mucous membranes of vertebrates. Based on the similarity of its L1 gene, there are more than 200 types divided into five groups (α, ß, γ, µ and ν) and the high oncogenic risk are HPV16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, and 59, with HPV 16 and 18 being present in 70% of invasive cervical cancer cases [10]. HPV infection is responsible for a spectrum of atypia and cytopathological lesions that favor cervical squamous cell carcinoma as Low-Grade Squamous Intraepithelial Lesions (LSILs), including Atypical Squamous Cells of Undetermined Significance (ASC-US) and CIN grade 1 (CIN1), High-Grade Intraepithelial Lesions (HSILs), and cervical carcinoma in situ [11,12].
The Brazilian health system offers the Pap smear test and HPV vaccination as the main measures for preventing cervical cancer. The DNA-HPV screening program and genotyping of oncogenic HPV types, although promising, is being discreetly introduced into public primary health care [13,14]; however, any health policies for C. trachomatis screening in the asymptomatic young population have not been established [15]. In Brazil, the prevalence of C. trachomatis varies from 2.2% to 10.8% [16,17,18,19,20,21] and that of HPV is 25.4% [22]. In the Amazon, the frequency of HPV varies from 15.5% to 63.3%, the highest rates of cervical cancer in the national territory [23,24,25,26]. University women in the Amazon region are characterized by being young women of reproductive age most likely to have risky sexual behavior and socioeconomic vulnerability and/or come from remote communities with poor access to higher education and gynecological health services [27,28,29]. In countries with very specific public screening and molecular diagnosis programs, preventive issues are well targeted when the profile of each population is considered. Knowledge of the prevalence and factors associated with endocervical infection by C. trachomatis and HPV in college women is important to understand the epidemiology of this infection and to plan prevention strategies targeted at this population. This study aimed to describe the prevalence and factors associated with endocervical infection by C. trachomatis and HPV in female students at the largest public university in the Brazilian Amazon region.

2. Materials and Methods

2.1. Type and Variables of Study

This is a pilot, cross-sectional analytical study that lasted from May 2018 to January 2020. Asymptomatic female university students, aged 18 or over, spontaneously attended by the Cytopathology Laboratory and Clinical Analysis Laboratory (LAC) of the Institute of Biological Sciences (ICB) of the Federal University of Para (UFPA), were invited to participate in the study. The inclusion criteria were female students regularly enrolled in undergraduate and graduate courses at the Federal University of Para, over 18 years old, who had initiated sexual activity. The exclusion criteria were menstruating or pregnant women, students who had undergone partial or total hysterectomy or with history of serious cervical injuries, in addition to those who did not wish to participate in the project and/or did not sign the free and informed consent form (FICF). The variables of this study were as follows: municipality of origin, age (years), marital status, family income (Brazilian minimum wages), number of children, alcohol use, having a public school background in basic education, coitarche (years), number of sexual partners in life, constant condom use, miscarriage, menarche, cytological conditions (LSISL/ASCUS, HSIL/ASC H, Normal), Pap test frequency, and HPV vaccination.

2.2. Collection and Analysis of Biological Sample (Endocervical Secretion)

Endocervical secretions were collected during the Pap smear using an endocervical brush, Ayres spatula, and a glass slide for subsequent analysis. The samples were stored in cryogenic tubes with 1 mL of Tris-EDTA (TE) buffered solution [10 mM Tris-HCl pH 8.5; 1 mM EDTA] at a temperature of −20 °C. During the Pap smear, the ectocervix and endocervix were scraped, the collected material was transferred to a glass slide previously identified and fixed with alcohol (96%). The usual Papanicolaou staining (Harris hematoxylin, Orange G and EA-36) was performed and subsequently analyzed by light microscopy. The results were classified as normal or atypical cells (atypia). Atypical cells of undetermined significance are divided according to their origin site: glandular (AGG) or squamous (ASC). Cells of squamous origin were also subdivided into Low-Grade Intraepithelial Lesion (LSIL, comprising HPV cytopathic effect and CIN I), high-grade intraepithelial lesion (HSIL, comprising CIN II and CIN III) and atypical squamous cells (ASCs). The high-grade lesions where microinvasion and carcinoma could not be excluded were classified as invasive squamous cell carcinoma. Glandular lesions were divided into adenocarcinoma in situ (AIS) and invasive adenocarcinoma. Conventional cytology results were classified using Bethesda terminology [30].

2.2.1. DNA Extraction

Genomic DNA extraction was performed using a pureLink genomic DNA purification kit (Invitrogen, Carlsbad, California, USA), following the manufacturer’s recommendations, and then, the samples were stored at −20 °C until further analysis. A Polymerase Chain Reaction (PCR) of the human β-globin gene was performed before detection of C. trachomatis and HPV to confirm sample suitability.

2.2.2. Amplification of the human β-globin Gene

All genomic DNA extracted was subjected to a PCR for amplification of a 268 bp fragment of the human β-globin gene to verify the quality of the extracted DNA. For this step, PC03/GH20 primers were used. The reaction consisted of 5 µL of GoTaq Green Master Mix (Promega Biotecnologia, Madison, Wisconsin, USA), 2.5 µL of H2O, 0.25 µL of each primer (0.5 µM), and 2 µL of extracted DNA. The temperature cycles had an initial denaturation at 94 °C for 4 min, followed by 35 cycles at 94 °C for 45 s, annealing at 55 °C for 45 s, and extension at 72 °C for 45 s, with a final extension at 72 °C for 8 min. PCR products were electrophoresed on a 2% agarose gel in 1× TAE buffer (100 V, 1 h), stained with Sybr Safe (4 µL), and visualized under ultraviolet light. Sterile water was included as a negative control to rule out contamination.

2.2.3. Detection of an ompA Gene Fragment from C. trachomatis

For the detection of endocervical infection by C. trachomatis, we performed a modified nested-PCR protocol [31], which amplifies a 394 pb pair fragment of the chromosomal ompA gene of C. trachomatis. For the first nested-PCR, we used 6.0 μL of GoTaq Green Master mix (Promega, Madison, WI, USA), 0.5 μL of primers P1 (A) (5′GACTTTGTTTTCGACCGTGTT-3′), and P2 (5′AGCRTATTGGAAAGAAGCBCCTAA-3′) with a concentration of 20 pmol/μL of each primer; in addition, we used 2 μL of genomic DNA and 3 μL of sterile water, resulting in a final volume of 12 μL. In the second nested-PCR, we used 0.5 μL of the amplified material from the first nested-PCR, 6.0 μL of Go Taq Green Master Mix (Promega, Madison, WI, USA), 4.5 μL of sterile water and 0.5 μL (20 pmol/μL) of primers P3 (5′-AAACWGATGTGAATAAAGARTT-3′) and P4 (5′-TCCCASARAGCTGCDCGAGC-3′). Positive and negative controls were used in all reactions to optimize the results of choosing the positive sample and to verify DNA contamination between the samples, respectively. In all nested-PCR, an initial temperature of 95 °C was considered, lasting five minutes in the first nested-PCR and 1 min in the second nested-PCR, followed by 35 cycles of denaturation at 94 °C for 40 s, annealing at 54 °C for 30 s and extension at 72 °C for 90 s, with a final extension step at 72 °C for 7 min. The amplified products were visualized by electrophoresis in a 1% agarose gel with 0.5 mg/mL ethidium bromide.

2.2.4. Detection of HPV L1 Gene Fragment

To detect HPV infection, we used the degenerate primers MY09/MY11, which amplify a fragment of the HPV L1 gene and have between 449 pb and 458 pb, depending on the HPV type. The sequences of the primers used were as follows: MY09 (5′-CGTCCMAARGGAWACTGATC-3′) and MY11 (5′-GCMCAGGGWCATAAYAATGG-3′), with the following correspondents: M = A + C, R = A + G, W = A + T, Y = C + T. For this step, 0.2 mL microtubes were used in an Applied Biosystems 2720 thermocycler. The final reaction volume was 10 µL [5 µL of Go Taq Green Master Mix 2X (CF = 1x), 1 µL of each primer (10 µM; CF = 1 µM), 2 µL of nuclease-free H2O and 2 µL of DNA]. The PCR followed the steps of initial denaturation at 94 °C for 2 min, followed by 35 cycles with denaturation at 94 °C for 45 s, primer hybridization at 55 °C for 45 s and chain extension at 72 °C for 45 s. Finally, the material was kept at 72 °C for 10 min (final extension). The positive control was a known positive sample (HPV16) and the negative control was nuclease-free water [32].

2.3. Ethical Aspects

The investigations were conducted in accordance with point 23 of the Declaration of Helsinki (1975, revised in 2013) and the Resolution 466/2012 of the National Health Council [33]. This study is part of the project “Detection and genotyping of C. trachomatis in university students treated at the cytopathology laboratory/UFPA: cytological and molecular analysis”, considering all regulations to ensure the ethics and confidentiality of the participants. Our research was authorized by the Research Ethics Committee of the Center for Tropical Medicine of the Federal University of Para (Registration: 103,571/CAAE 07821212,2,0000,5172) Approved on 19 September 2012. Only college women over 18 years old who read and signed the free and informed consent form (ICF) before the collection of biological samples and socioepidemiological and gynecological data were included in this study. All data were analyzed with full anonymity. Participants who tested positive for sexually transmitted infection with C. trachomatis were referred for medical evaluation.

2.4. Statistical Analysis

The Statistical Package for Social Sciences (SPSS) version 21.0 (SPSS, Chicago, IL, USA) was used for the analyses. The chi-square, Fisher’s exact, and Odds Ratio tests were used to analyze categorical variables with only two options. The G test of independence was used for variables with more than two options in all our analyses of comparisons between the variables and the positivity of C. trachomatis and HPV infection. For variables with more than two options, the G test of independence was used along with Cramer’s V test to verify the effect size of these variables, in which the level of association was defined as weak (less than or equal to 0.29), moderate (0.30 to 0.49), or strong (0.50 or greater). Multiple logistic regression was used to reduce the chances of bias. We considered for this study a 95% confidence interval (CI) and a significance level of p ≤ 0.05.

3. Results

In this study, 52% (157/302) of the participants were 25 years old or older, 90.7% (274/302) were single, 72.2% (218/302) had a family income of one to three Brazilian minimum wages, 80.1% (242/302) had no children, 60.6% (183/302) consumed alcohol, 84.1% (254/302) had a public school education, 76.2% (232/302) had sexual life after 15 years of age, 84.1% (254/302) had more than one sexual partner in their lifetime, 72.9% (220/302) did not use condoms during sexual intercourse, 88.7% (268/302) had never had miscarriage, and 96.7% (292/302) had menarche at an age greater than 15 years (Table 1). In this study, the number of participants per municipality of origin was variable, concentrating in the capital Belém (N = 220), and in the interior: Ananindeua (n = 54), Marituba (n = 11), Abaetetuda (n = 3), Castanhal (n = 3), Acará (n = 3), Santa Izabel (n = 3); there was also one participant from each of these municipalities: Barcarena, Benevides, Moju, Santo Antônio do Tauá and Tome-Açu (Figure 1).
The overall prevalence of endocervical infection by C. trachomatis was 8.3% (25/302) and by HPV was 28.9% (87/302) in our entire study population. Cases of coinfection were 3.3% (10/302), all from women living in the capital (Table 1).
The participants’ median age was 25 years old (interquartile range: 22.0–29.25 years, range: 18–55 years). Among the female undergraduates who tested positive for endocervical infection by C. trachomatis and HPV, the median age was 23 years old (interquartile range: 21–26 years, range: 18–51 years) and 23 years old (interquartile range: 21–26 years, range: 18–55 years), respectively. Women who reported earning less than one Brazilian minimum wage were significantly associated with sexually transmitted infection by C. trachomatis (14.8%, p = 0.0497). College women under 25 years old were twice as likely to acquire HPV infection [39.3%, (OR: 2.6989), CI95%: 1.6054–4.5371, p = 0.0002], as were women who reported not having children [31.8%, (OR: 2.333), CI: 1.1235–4.8461, p = 0.0307]. Being a college student who did not attend a public school during basic education reduced the chances of acquiring this STI by 63% compared to those who came from a public school [45.8% (OR: 0.3713), CI: 0.1951–0.7064, p = 0.0035]. There was no significant difference between the prevalence of endocervical infections by C. trachomatis and HPV in students from the capital and those from the interior of Para (Table 2).
We did not observe a significant association between the variable’s cytological conditions, Pap smear performance and HPV vaccination; however, we observed that HSIL/ASC-H was the most common cytological condition among HPV-positive participants (54.5%) (Table 3).

4. Discussion

In this study, a high prevalence of endocervical infection by C. trachomatis (8.3%) was found in female students at the largest public university in the Amazon region of Brazil. Brazil’s universal health system has not yet created a screening policy for C. trachomatis in the asymptomatic young female population under 25 years old [15], so we do not know how to measure the total number of cases at the national level. However, the prevalence of C. trachomatis in Brazil ranges from 2.2% to 10.8% [16,17,18,19,20,21] and similar prevalence rates have been found in university students in the Brazilian Amazon [29] and in other cities such as Mbeya-Tanzania (11%) [34], Wisconsin, United States (7.2%) [35], and in Uppsala, Sweden [36] which, like in our study, report that socioeconomic vulnerability generated by poverty supports a large part of the social risk conditions for acquiring STIs caused by C. trachomatis [37].
In Brazil, gynecological health services in primary care operate with great logistical, structural and financing difficulties for the low-income population [28], and the impacts of this situation can be observed in the high rates of hospitalization for PID [38,39]; this is probably the reason why the participants who had a family income below the Brazilian minimum wage (equivalent to USD 250) were significantly associated with C. trachomatis infection (p = 0.0497). Public universities in the Amazon are an open space that receives a great diversity of people from different social standards; about 70.2% of them are composed of low-income people [40] and many of them receive financial aid to support themselves in the capital [41]. This study showed high prevalence of endocervical HPV infection (28.9%) comparable with the national HPV burden, which is 25.4% to 54% [22,42], as well as the burden in college women in Brazil [22,27,43] and in university students from Maputo, Mozambique (28.6%) [44], Vietnam (4.0%) [45], and Gaborone, Botswana (31%) [46]. HPV rates from 15.5% to 63.3% have been detected in the Amazon [9,17,21] and even during the establishment of public measures to control and prevent this infection, this region has the highest number of cases of cervical cancer and low anti-HPV vaccine adherence [47].
Young age is a major risk factor for STIs, as it is a phase of life in which women acquire new perceptions, with changes in feelings and the search for new experiences to form their personal identity. These aspects interfere in their sexual life, and high rates of STIs are often associated with risky sexual behavior [48]. In the present study, the results showed that university girls under 25 years old were twice as likely to acquire the HPV infection (OR: 2.6989, p = 0.0002). Childless women were twice as likely to acquire endocervical HPV infection compared to those with children (OR: 2.333, p = 0.0307), which is a consequence of the risky sexual behavior admitted by these young women, who, because they do not have children, and possibly not even a stable relationship and/or steady partner, feel free to experiment variable sexual practices and new partners [49]. In this case, sexually active young college women may be unassisted by public preventive health services and health education on STIs, unlike women with children who generally have a steady sexual partner and had preventive medical monitoring for HPV during pregnancy in prenatal care [50,51].
Sexual education about STIs and vaccination against HPV are mandatory for adolescents and young adults in primary and secondary schools in Brazil, through the Brazilian National Curricular Guidelines for Education [52] and parallel actions by the Brazilian Government through the Health in School Program [53].
In our study, college women who did not come from public schools had a 63% reduced chance of acquiring HPV infection when compared to the participants who came from public schools (OR: 0.3713, p = 0.0035), because young women who studied in public schools in previous years are low-income and suffer the impacts of socioeconomic fragility and difficulty in receiving medical care and accepting vaccinations, either because they are from peripheral populations of the capital or from remote communities [54].
The limitations of this study are the low sample size obtained mainly among students who came from cities in the interior of the state of Para. We did not investigate the circulating genotypes of both infections, which made it impossible for us to perform epidemiological analyses according to the genotypic distribution pattern to attempt any comparison with the cytological conditions. The low student participation rate is possibly due to a lack of awareness among students, fear or stigma associated with participating in an STI study, or limited access to health care due to socioeconomic barriers. The sampling bias is possible because the university students answered the questionnaire according to socially shaped measures, distorting the true condition of the socioepidemiological indicators of the infection.

5. Conclusions

Endocervical infection by C. trachomatis was significantly present in college women who had a family income below the Brazilian minimum wage and students under 25 years old. Women who did not have children were twice as likely to acquire endocervical HPV infection, and participants who did not study in a public school during basic education had a significantly reduced risk of HPV infection. Further studies will be important to understand the distribution of C. trachomatis and HPV genotypes and their clinical implications in Amazonian populations. STI prevention policies need to be intensified for the female population of young university students in the Amazon region to understand the epidemiological patterns of these infections and ensure future control and prevention of secondary pathologies such as PID and cervical cancer.

Author Contributions

Conceptualization: R.C.V. and L.d.S.C.C. Data curation: L.M.d.S., K.V.B.L. and M.C.M.d.S. Investigation and methodology: R.V.D.S., L.M.d.S. and G.M.M.d.M. Formal analysis: R.V.D.S. and T.d.M.B. Writing—original draft: L.M.d.S. and R.V.D.S. Writing—review and editing: L.M.d.S. Project administration: R.V.D.S., E.A.Y.I. and M.S.d.S. All authors have read and agreed to the published version of the manuscript.

Funding

This project was funded by the Foundation for Support and Development of Research–FADESP (Project_3698_UFPA/FADESP_2015).

Institutional Review Board Statement

The investigations were conducted in accordance with the Declaration of Helsinki (1975, revised in 2013), according to point 23 of this declaration and in compliance with Resolution 466/2012 of the National Health Council [33]. This study is part of the project “Detection and genotyping of C. trachomatis in university students treated at the cytopathology laboratory/UFPA: cytological and molecular analysis”, considering all regulations to ensure the ethics and confidentiality of the participants. Our research was authorized by the Research Ethics Committee of the Center for Tropical Medicine of the Federal University of Para (Registration: 103,571/CAAE 07821212,2,0000,5172). Approved on 19 September 2012.

Informed Consent Statement

In all cases, only college women over 18 years old who read and signed the free and informed consent form (ICF) before the collection of biological samples and socioepidemiological and gynecological data were included in this study. All data were analyzed with full anonymity. Participants who tested positive for sexually transmitted infection with C. trachomatis were referred for medical evaluation.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Acknowledgments

Pro-Rectory of Extension of the Federal University of Pará.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. World Health Organization. Final Global Health Sector Strategies on Respectively, HIV, Viral Hepatitis and Sexually Transmitted Infections, 2022–2030. Global HIV, Hepatitis and STIs Programmes. 2022. Available online: https://www.who.int/teams/global-hiv-hepatitis-and-stis-programmes/strategies/global-health-sector-strategies (accessed on 20 March 2025).
  2. Bruni, L.; Albero, G.; Rowley, J.; Alemany, L.; Arbyn, M.; Giuliano, A.R.; Markowitz, L.E.; Broutet, N.; Taylor, M. Global and regional estimates of genital human papillomavirus prevalence among men: A systematic review and meta-analysis. Lancet Glob. Health 2023, 11, e1345–e1362. [Google Scholar] [CrossRef]
  3. Sangpichai, S.; Patarapadungkit, N.; Pientong, C.; Ekalaksananan, T.; Chaiwiriyakul, S.; Thongbor, R.; Sirivech, P.; Jangsiriwitayakorn, P.; Triamwittayanon, T. Chlamydia trachomatis infection in high-risk human papillomavirus based on cervical cytology specimen. Asian Pac. J. Cancer Prev. 2019, 20, 3843–3847. [Google Scholar] [CrossRef] [PubMed][Green Version]
  4. Bhuvanendran Pillai, A.; Mun Wong, C.; Dalila Inche Zainal Abidin, N.; Fazlinda Syed Nor, S.; Fathulzhafran Mohamed Hanan, M.; Rasidah Abd Ghani, S.; Afzan Aminuddin, N.; Safian, N. Chlamydia Infection as a Risk Factor for Cervical Cancer: A Systematic Review and Meta-Analysis. Iran. J. Public Health 2022, 51, 508–517. [Google Scholar] [CrossRef] [PubMed]
  5. Maueia, C.; Murahwa, A.; Manjate, A.; Sacarlal, J.; Kenga, D.; Unemo, M.; Andersson, S.; Mussá, T.; Williamson, A.L. The relationship between selected sexually transmitted pathogens, HPV and HIV infection status in women presenting with gynaecological symptoms in Maputo City, Mozambique. PLoS ONE 2024, 19, e0307781. [Google Scholar] [CrossRef] [PubMed]
  6. Elwell, C.; Mirrashidi, K.; Engel, J. Chlamydia cell biology and pathogenesis. Nat. Rev. Microbiol. 2016, 14, 385–400. [Google Scholar] [CrossRef]
  7. Tang, W.; Mao, J.; Li, K.T.; Walker, J.S.; Chou, R.; Fu, R.; Chen, W.; Darville, T.; Klausner, J.; Tucker, J.D. Pregnancy and fertility-related adverse outcomes associated with Chlamydia trachomatis infection: A global systematic review and meta-analysis. Sex. Transm. Infect. 2020, 96, 322–329. [Google Scholar] [CrossRef] [PubMed]
  8. Shroff, S. Infectious Vaginitis, Cervicitis, and Pelvic Inflammatory Disease. Med. Clin. N. Am. 2023, 107, 299–315. [Google Scholar] [CrossRef]
  9. Rodrigues, R.; Sousa, C.; Barros, A.; Vale, N. Chlamydia trachomatis: From Urogenital Infections to the Pathway of Infertility. Genes 2025, 16, 205. [Google Scholar] [CrossRef]
  10. Lizano, M.; Berumen, J.; García-Carrancá, A. HPV-related carcinogenesis: Basic concepts, viral types and variants. Arch. Med. Res. 2009, 40, 428–434. [Google Scholar] [CrossRef]
  11. Zhong, G.; Wang, Y.; Xie, Q.; Lin, R.; Yao, T. HPV-specific risk assessment of cervical cytological abnormalities. BMC Cancer 2021, 21, 949. [Google Scholar] [CrossRef]
  12. Wang, M.; Liang, H.; Yan, Y.; Bian, R.; Huang, W.; Zhang, X.; Nie, J. Distribution of HPV types among women with HPV-related diseases and exploration of lineages and variants of HPV 52 and 58 among HPV-infected patients in China: A systematic literature review. Hum. Vaccines Immunother. 2024, 20, 2343192. [Google Scholar] [CrossRef]
  13. Teixeira, J.C.; Vale, D.B.; Campos, C.S.; Bragança, J.F.; Discacciati, M.G.; Zeferino, L.C. Organization of cervical cancer screening with DNA-HPV testing impact on early-stage cancer detection: A population-based demonstration study in a Brazilian city. Lancet Reg. Health Am. 2021, 5, 100084. [Google Scholar] [CrossRef]
  14. Brasil. Portaria Sectics/MS Nº 3, de 7 de Março de 2024. Ministério da Saúde/Secretaria de Ciência, Tecnologia e Inovação e do Complexo Econômico-Industrial da Saúde. Diário Oficial da União. 2024. Available online: https://bvsms.saude.gov.br/bvs/saudelegis/sctie/2024/prt0003_08_03_2024.html (accessed on 10 April 2025).
  15. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento de HIV/Aids, Tuberculose, Hepatites Virais e Infecções Sexualmente Transmissíveis. Diretrizes e Estratégias Para o Enfrentamento ao HIV/Aids e Outras ISTs Para Mulheres em Situação de Vulnerabilidades [Recurso Eletrônico]. 2023. Available online: https://www.gov.br/aids/pt-br/central-de-conteudo/publicacoes/2023/diretrizes-e-estrategias-para-o-enfrentamento-ao-hiv_aids-e-outras-ists-para-mulheres-em-situacao-de-vulnerabilidades.pdf (accessed on 10 April 2025).
  16. Santos, L.M.; Vieira, M.R.M.D.S.; Oliveira, J.F.G.; Trindade, J.Q.; Brasiliense, D.M.; Ferrari, S.F.; Tsutsumi, M.Y.; Fuzii, H.T.; Sousa Junior, E.C.; Ishikawa, E.A.Y.; et al. High prevalence of sexual Chlamydia trachomatis infection in young women from Marajo Island, in the Brazilian Amazon. PLoS ONE 2018, 13, e0207853. [Google Scholar] [CrossRef] [PubMed]
  17. Link, R.A.; Link, C.A.; Benin Lima, M.H.; Pasetti, B.W.; Savaris, R.F. Prevalence of Chlamydia trachomatis in Women Who Are Candidates for In Vitro Fertilization in a Private Reference Service in Southern Brazil: A Cross-Sectional Study. Cureus 2022, 14, e24109. [Google Scholar] [CrossRef] [PubMed]
  18. Campaner, A.B.; de Castro, M.A.; Lucarelli, A.P. Chlamydia trachomatis prevalence in females in Sao Paulo, Brazil: 11 years’ surveillance of the infection. Braz. J. Microbiol. 2023, 54, 151–158. [Google Scholar] [CrossRef] [PubMed]
  19. Miranda, A.E.; Gaspar, P.C.; Schörner, M.A.; Barazzetti, F.H.; Dias, G.B.; Bigolin, A.; Pascom, A.R.P.; Barreira, D.; Bazzo, M.L.; Brazilian Surveillance for STIs in Pregnant Women Group. Prevalence of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Mycoplasma genitalium and risk factors among pregnant women in Brazil: Results from the national molecular diagnosis implementation project. Int. J. Gynaecol. Obstet. 2024, 166, 71–79. [Google Scholar] [CrossRef]
  20. Rocha, D.; Moraes, C.O.; Araújo, A.F.; Dos Santos Beltrão, Ê.; Castelo Dos Santos, L.; Menezes da Mata, L.; Nn Xavier, A.; Dos Santos Reis, R.; Cc Soares, S.; LTorres, K.; et al. Chlamydia trachomatis infection in women living in remote areas in Amazonas, Brazil-a self-collection screening experience. Int. J. STD AIDS 2019, 30, 336–343. [Google Scholar] [CrossRef]
  21. Correa Porto, C.R.C.; Longatto-Filho, A.; De Almeida, B.C.; Bonetti, T.C.; Kamaiurá, S.F.A.; Diaz, R.S.; Heinke, T.; Cury, F.P.; Santana, I.V.V.; Queiroz, M.M.; et al. Chlamydia trachomatis, Neisseria gonorrhoeae and human papillomavirus infections of lower genital tract of Indigenous women from Xingu Indigenous Park. Rural. Remote Health 2023, 23, 7126. [Google Scholar] [CrossRef]
  22. Colpani, V.; Soares Falcetta, F.; Bacelo Bidinotto, A.; Kops, N.L.; Falavigna, M.; Serpa Hammes, L.; Schwartz Benzaken, A.; Kalume Maranhão, A.G.; Domingues, C.M.A.S.; Wendland, E.M. Prevalence of human papillomavirus (HPV) in Brazil: A systematic review and meta-analysis. PLoS ONE 2020, 15, e0229154. [Google Scholar] [CrossRef]
  23. Monteiro, J.C.; Fonseca, R.R.S.; Ferreira, T.C.S.; Rodrigues, L.L.S.; Silva, A.R.B.; Gomes, S.T.; Silvestre, R.V.D.; Silva, A.N.R.; Pamplona, I.; Vallinoto, A.C.R.; et al. Prevalence of High Risk HPV in HIV-Infected Women from Belém, Pará, Amazon Region of Brazil: A Cross-Sectional Study. Front. Public Health 2021, 9, 649152. [Google Scholar] [CrossRef]
  24. Monteiro, J.C.; Tsutsumi, M.Y.; Carvalho, D.O.; Costa, E.C.S.; Feitosa, R.N.F.; Laurentino, R.V.; Fonseca, R.R.F.S.; Silvestre, R.V.D.; Oliveira-Filho, A.B.; Machado, L.F.A. Prevalence, Diversity, and Risk Factors for Cervical HPV Infection in Women Screened for Cervical Cancer in Belém, Pará, Northern Brazil. Pathogens 2022, 11, 960. [Google Scholar] [CrossRef] [PubMed]
  25. Santos, L.M.; de Souza, J.D.; Mbakwa, H.A.; Nobre, A.F.S.; Vieira, R.C.; Ferrari, S.F.; Rodrigues, A.R.; Ishikawa, E.A.Y.; Guerreiro, J.F.; de Sousa, M.S. High prevalence of sexual infection by human papillomavirus and Chlamydia trachomatis in sexually-active women from a large city in the Amazon region of Brazil. PLoS ONE 2022, 17, e0270874. [Google Scholar] [CrossRef]
  26. Rodrigues, L.L.S.; Pilotto, J.R.; Martinelli, K.G.; Nicol, A.F.; Paula, V.S.; Gheit, T.; Oliveira, N.S.C.; Silva-de-Jesus, C.; Sahasrabuddhe, V.V.; Silva, D.M.; et al. Diversity of Anal HPV and Non-HPV Sexually Transmitted Infections and Concordance with Genital Infections in HIV-Infected and HIV-Uninfected Women in the Tapajós Region, Amazon, Brazil. Viruses 2023, 15, 1328. [Google Scholar] [CrossRef]
  27. Vieira, R.C.; Monteiro Jdo, S.; Manso, E.P.; Dos Santos, M.R.; Tsutsumi, M.Y.; Ishikawa, E.A.; Ferrari, S.F.; Lima, K.V.; de Sousa, M.S. Prevalence of type-specific HPV among female university students from northern Brazil. Infect. Agent Cancer 2015, 10, 21. [Google Scholar] [CrossRef]
  28. Machado, L.F.A.; Fonseca, R.R.S.; Queiroz, M.A.F.; Oliveira-Filho, A.B.; Cayres-Vallinoto, I.M.V.; Vallinoto, A.C.R.; Ishak, M.O.G.; Ishak, R. The Epidemiological Impact of STIs among General and Vulnerable Populations of the Amazon Region of Brazil: 30 years of Surveillance. Viruses 2021, 13, 855. [Google Scholar] [CrossRef] [PubMed]
  29. Santos, L.M.; Vieira, M.R.M.D.S.; Vieira, R.C.; Silva, L.B.D.L.; de Macêdo, G.M.M.; Miranda, A.E.; Brasiliense, D.M.; EGuimarães, R.J.P.S.; Sousa ECJunior Ferrari, S.F.; Pinheiro, H.H.C.; et al. Prevalence and circulant genotypes of Chlamydia trachomatis in university women from cities in the Brazilian Amazon. PLoS ONE 2024, 19, e0287119. [Google Scholar] [CrossRef] [PubMed]
  30. Alrajjal, A.; Pansare, V.; Choudhury, M.S.R.; Khan, M.Y.A.; Shidham, V.B. Squamous intraepithelial lesions (SIL: LSIL, HSIL, ASCUS, ASC-H, LSIL-H) of Uterine Cervix and Bethesda System. Cytojournal 2021, 18, 16. [Google Scholar] [CrossRef] [PubMed]
  31. Jalal, H.; Stephen, H.; Alexander, S.; Carne, C.; Sonnex, C. Development of real-time PCR assays for genotyping of Chlamydia trachomatis. J. Clin. Microbiol. 2007, 45, 2649–2653. [Google Scholar] [CrossRef] [PubMed][Green Version]
  32. Manos, M.M.; Ting, Y.; Wright, D.K.; Lewis, A.J.; Broker, T.R.; Wolinsky, S.M.; Shin, Y.T. The use of polymerase chain reaction amplification for the detection of genital human papillomaviruses. Cancer Cells 1989, 7, 209–214. [Google Scholar]
  33. Conselho Nacional de Saúde (Brasil). Resolução nº 466, de 12 de Dezembro de 2012. Brasília. Available online: http://www.conselho.saude.gov.br/web_comissoes/conep/index.html (accessed on 25 April 2022).
  34. Mcharo, R.D.; Kisinda, A.; Njovu, L.; Mcharo, M.; Mbwilo, F.; Mihale, G.; Komba, B.; Andrew, E.; Mayaud, P.; Kroidl, A.; et al. Prevalence of and risk factors associated with HIV, Herpes Simplex Virus-type 2, Chlamydia trachomatis and Neisseria gonorrhoeae infections among 18–24 year old students attending Higher Learning Institutions in Mbeya-Tanzania. PLoS ONE 2022, 17, e0266596. [Google Scholar] [CrossRef]
  35. Sienkiewicz, L.; Thomas, Y.; Reynoso, A.; Munson, E. Incidence and laboratory diagnosis of sexually-transmitted infections among university students in a high-prevalence community. J. Am. Coll. Health 2023, 71, 571–577. [Google Scholar] [CrossRef]
  36. Smeds, S.; Obern, C.; Poromaa, I.S.; Westerbergh, J.; Tydén, T.; Gyllenberg, F. Self-reported sexually transmitted infections and associated risk factors among female university students. Upsala J. Med. Sci. 2024, 129. [Google Scholar] [CrossRef] [PubMed]
  37. Fortas, C.; Delarocque-Astagneau, E.; Randremanana, R.V.; Crucitti, T.; Huynh, B.T. Asymptomatic infections with Chlamydia trachomatis, Neisseria gonorrhoeae, and Trichomonas vaginalis among women in low- and middle-income countries: A systematic review and meta-analysis. PLoS Glob. Public Health 2024, 4, e0003226. [Google Scholar] [CrossRef] [PubMed]
  38. Suehiro, T.T.; Gimenes, F.; Souza, R.P.; Taura, S.K.I.; Cestari, R.C.C.; Irie, M.M.T.; Boer, C.G.; Consolaro, M.E.L.; Silva, V.R.S.D. High molecular prevalence of HPV and other sexually transmitted infections in a population of asymptomatic women who work or study at a Brazilian university. Rev. Inst. Med. Trop. Sao Paulo 2021, 63, e1. [Google Scholar] [CrossRef]
  39. Perciney, P.; Costa, A.L.S.; Leite, I.C.G.; Nogueira, M.C. Pelvic inflammatory disease hospitalizations in Brazil: Time trend from 2000 to 2019. Rev. Bras. Saúde Mater. Infant. 2022, 22, 767–773. [Google Scholar] [CrossRef]
  40. Hartmann, Y.; de Cássia Cde AAkutsu, R.; Zandonadi, R.P.; Raposo, A.; BABotelho, R. Characterization, Nutrient Intake, and Nutritional Status of Low-Income Students Attending a Brazilian University Restaurant. Int. J. Environ. Res. Public Health 2021, 18, 315. [Google Scholar] [CrossRef]
  41. Brasil. Ministério da Educação. MEC Garante Assistência Para Alunos Permanecerem na Graduação. Educação Superior. 2025. Available online: https://www.gov.br/mec/pt-br/assuntos/noticias/2025/fevereiro/mec-garante-assistencia-para-alunos-permanecerem-na-graduacao#:~:text=A%20Pnaes%20fortalece%20a%C3%A7%C3%B5es%20anteriores,a%20verba%20destinada%20em%202022 (accessed on 21 April 2025).
  42. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Departamento do Programa Nacional de Imunizações. Estratégia de Vacinação na Escola: 2025 [Recurso Eletrônico]. 2025. Available online: https://www.gov.br/saude/pt-br/vacinacao/publicacoes/estrategia-de-vacinacao-nas-escolas-2025.pdf/view (accessed on 25 April 2025).
  43. Burlamaqui, J.C.; Cassanti, A.C.; Borim, G.B.; Damrose, E.; Villa, L.L.; Silva, L. Human Papillomavirus and students in Brazil: An assessment of knowledge of a common infection—preliminary report. Braz. J. Otorhinolaryngol. 2017, 83, 120–125. [Google Scholar] [CrossRef]
  44. Bule, Y.P.; Silva, J.; Carrilho, C.; Campos, C.; Sousa, H.; Tavares, A.; Medeiros, R. Human papillomavirus prevalence and distribution in self-collected samples from female university students in Maputo. Int. J. Gynaecol. Obstet. 2020, 149, 237–246. [Google Scholar] [CrossRef] [PubMed]
  45. Van Trang, N.; Prem, K.; Toh, Z.Q.; Viet Ha, B.T.; Ngoc Lan, P.T.; Tran, H.P.; Pham, Q.D.; VANKhuu, N.; Jit, M.; Luu, D.T.; et al. Prevalence and Determinants of Vaginal Infection with Human Papillomavirus Among Female University Students in Vietnam. In Vivo 2022, 36, 241–250. [Google Scholar] [CrossRef]
  46. Ramogola-Masire, D.; McClung, N.; Mathoma, A.; Gargano, J.W.; Nyepetsi, N.G.; Querec, T.D.; Onyekwuluje, J.; Mine, M.; Morroni, C.; Luckett, R.; et al. Human papillomavirus prevalence in male and female university students in Gaborone, Botswana. Epidemiol. Infect. 2022, 150, e87. [Google Scholar] [CrossRef]
  47. Mendes Lobão, W.; Duarte, F.G.; Burns, J.D.; de Souza Teles Santos, C.A.; Chagas de Almeida, M.C.; Reingold, A.; Duarte Moreira, E., Jr. Low coverage of HPV vaccination in the national immunization programme in Brazil: Parental vaccine refusal or barriers in health-service based vaccine delivery? PLoS ONE 2018, 13, e0206726. [Google Scholar] [CrossRef] [PubMed]
  48. Desrosiers, A.; Betancourt, T.; Kergoat, Y.; Servilli, C.; Say, L.; Kobeissi, L. A systematic review of sexual and reproductive health interventions for young people in humanitarian and lower-and-middle-income country settings. BMC Public Health 2020, 20, 666. [Google Scholar] [CrossRef] [PubMed]
  49. Woods, H.E.; Schuh, A.M.; Gaydos, C.A.; Fenchel, M.; Kowalczyk Mullins, T.L.; Conard, L.A.E.; Manabe, Y.C.; Widdice, L.E. Preferences for Rectal Sexually Transmitted Infection Sample Collection and Sexual Behaviors Among Adolescent and Young Adult Women Accessing Primary Care Services. Sex. Transm. Dis. 2023, 50, 613–618. [Google Scholar] [CrossRef]
  50. Neves, R.G.; Flores-Quispe, M.D.P.; Facchini, L.A.; Fassa, A.G.; Tomasi, E. Prenatal care in Brazil: A cross-sectional study of the Program for Improving Primary Care Access and Quality, 2014. Epidemiol. Serv. Saude. 2020, 29, e2019019. [Google Scholar] [CrossRef]
  51. Freitas, F.M.D.S.; Correia, R.D.G.C.F.; Biazus-Dalcin, C.; Jorge, H.M.F.; Aquino, P.S.; Oliveira, B.L.C.A. Prenatal tests in Brazil: Prevalence and associated factors according to the Brazilian National Health Survey. Rev. Esc. Enferm. USP 2025, 58, e20240154. [Google Scholar] [CrossRef]
  52. Brasil. Ministério da Educação. Secretaria de Educação Básica. Secretaria de Educação Continuada, Alfabetização, Diversidade e Inclusão. Secretaria de Educação Profissional e Tecnológica. Conselho Nacional da Educação. Câmara Nacional de Educação Básica. Diretrizes Curriculares Nacionais Gerais da Educação Básica. ISBN 978-857783-136-4. Available online: https://www.gov.br/mec/pt-br/acesso-a-informacao/media/seb/pdf/d_c_n_educacao_basica_nova.pdf (accessed on 25 April 2025).
  53. Brasil. Presidência da República. Decreto n.º 6.286, de 5 de dezembro de 2007. Institui o Programa Saúde na Escola—PSE, e dá outras providências. Brasília. 2007. Available online: https://www.planalto.gov.br/ccivil_03/_ato2007-2010/2007/decreto/d6286.htm (accessed on 25 April 2025).
  54. Silva, I.A.G.; Sá, A.C.M.G.N.; Prates, E.J.S.; Malta, D.C.; Matozinhos, F.P.; Silva, T.M.R.D. Vaccination against human papillomavirus in Brazilian schoolchildren: National Survey of School Health, 2019. Rev. Lat. Am. Enfermagem. 2022, 30, e3834. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Number of college women by their respective municipalities of origin in the state of Para, Amazon region of Brazil.
Figure 1. Number of college women by their respective municipalities of origin in the state of Para, Amazon region of Brazil.
Microorganisms 14 01176 g001
Table 1. Comparison of the prevalence of endocervical infection by C. trachomatis and HPV in college women from the capital (Belem) and the interior of the state of Para, Amazon, Brazil.
Table 1. Comparison of the prevalence of endocervical infection by C. trachomatis and HPV in college women from the capital (Belem) and the interior of the state of Para, Amazon, Brazil.
Prevalence by Municipality of OriginTotal
(n = 302)
C. trachomatis (+) (N = 25)ORCI (95%)p-ValueHPV (+) (N = 87)ORCI (95%)p-Value
N%N%2.92590.8517–10.05210.1226N%1.14570.6481–2.01880.7484
Interior8227.233.5 2226.8
Capital22072.82210 6529.6
Descriptive data on the prevalence of C. trachomatis and HPV infection. OR: Odds ratio. CI (95%): 95% confidence interval. C. trachomatis (+): C. trachomatis positive. HPV (+): HPV-positive. n: Total number of the study population; N: Number of the specific stratified population for both C. trachomatis positive and HPV positive cases.
Table 2. Prevalence, socioepidemiological characteristics, and sexual behavior of college women in the state of Pará, Amazon, Brazil.
Table 2. Prevalence, socioepidemiological characteristics, and sexual behavior of college women in the state of Pará, Amazon, Brazil.
Variables Total (n = 302)CT (+)
N = 25 (8.3%)
ORCI (95%)p-Valuep-Value ±HPV (+)
N = 87 (28.9%)
ORCI (95%)p-Valuep-Value ±
N%N%N%
Age (years)  a<25145481510.31.64720.7155–3.79450.33010.23425739.32.69891.6054–4.53710.0002 *0.0049 *
≥2515752106.4 3019.1
Marital status  aSingle27490.7228.10.66400.1847–2.38730.79580.12058229.91.79380.6840–5.10630.31030.7886
Married289.3310.7 517.8
Family incomec<15417.9814.80.119 †--0.0497 *1425.90.022 †--0.6598
1–321872.2167.3 6228.5
>3309.913.3 1136.6
Children  bNo24280.1229.11.90000.5493–6.57200.44260.18427731.82.33330.1235–4.84610.0307 *0.0482 *
Yes6019.935 1016.6
Alcohol  aYes18360.694.90.85400.3645–2.00080.88080.65843217.40.85600.5120–1.43100.64320.6826
No11939.41613.4 5546.2
From public school  aYes25484.1197.50.53450.2012–1.41990.32540.19686525.60.37130.1951–0.70640.0035 *0.0178 *
No4815.9612.5 2245.8
Age of first intercourse (years)≤157023.857.10.81540.2944–2.25810.88400.411221301.07790.6003–1.93560.91980.6768
>1523276.2208.6 6628.4
Number of sexual partners in life  b14815.924.20.60680.1385–2.65930.72340.624512250.79560.3924–1.61290.64450.9309
>125484.1239.1 7529.5
Constant condom
use  b
Yes8227.156.11.48510.5381–4.09890.59530.47712429.20.92450.5280–1.61880.89610.8909
No22072.9209.1 6328.6
Miscarriage  bYes3411.3411.80.53230.1760–1.60260.36920.11481029.41.03350.4720–2.26310.76350.4407
No26888.7217.8 7728.7
Menarche  b≤1529296.7248.20.71380.0856–5.94880.76350.87478629.43.32370.4094–26.98050.41420.8620
>15103.3110 110
CT: C. trachomatis. a Chi-square test, b Fisher’s exact, c G test. † Equivalent to Brazilian minimum wage. OR: Odds Ratio. CI (95%): ± Multiple Logistic Regression. † Cramer’s V test for variables with more than two lines considering level of association as weak (≤0.29), moderate (0.3–0.49) or strong (≥0.5). Confidence interval of 95%. CT (+): C. trachomatis positive. HPV (+): HPV-positive. *: statistically significant p-value. n: Total number of the study population; N: Number of the specific stratified population for both C. trachomatis positive and HPV positive cases.
Table 3. Pap smear results of college women from the state of Para, Amazon, Brazil.
Table 3. Pap smear results of college women from the state of Para, Amazon, Brazil.
Cytological and HPV Vaccination ConditionsTotal
(n = 302)
CT (+) (N = 25)ORCI (95%)p-ValueHPV (+)
(n = 87)
ORCI (95%)p-Value
N%N% N%
Cytological conditions LSISL/ASCUS196.3210.5--0.9920 G736.8--0.1418 G
HSIL/
ASC H
113.619.1 654.5
Normal27290.1228.1 7427.2
Pap smear annuallyYes21571.2209.31.68210.6106–4.63390.43266329.31.08810.6250–1.89400.8745
No8728.855.7 2427.5
HPV VaccinationYes8026.5-----28351.48760.8604–2.57200.1997
No22273.5-----5926.6
CT: C. trachomatis. OR: Odds Ratio. G: G test. CI (95%): Confidence interval of 95%. CT (+): C. trachomatis positive. HPV (+): HPV-positive. n: Total number of the study population; N: Number of the specific stratified population for both C. trachomatis positive and HPV positive cases.
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Santos, L.M.d.; Vieira, R.C.; de Souza Canto Covre, L.; da Silva, M.C.M.; Bezerra, T.d.M.; de Macedo, G.M.M.; Ishikawa, E.A.Y.; Lima, K.V.B.; de Sousa, M.S.; Silvestre, R.V.D. High Burden of Chlamydia trachomatis and Human Papillomavirus Infections in Low-Income Female University Students from Public Schools in the Brazilian Amazon. Microorganisms 2026, 14, 1176. https://doi.org/10.3390/microorganisms14061176

AMA Style

Santos LMd, Vieira RC, de Souza Canto Covre L, da Silva MCM, Bezerra TdM, de Macedo GMM, Ishikawa EAY, Lima KVB, de Sousa MS, Silvestre RVD. High Burden of Chlamydia trachomatis and Human Papillomavirus Infections in Low-Income Female University Students from Public Schools in the Brazilian Amazon. Microorganisms. 2026; 14(6):1176. https://doi.org/10.3390/microorganisms14061176

Chicago/Turabian Style

Santos, Leonardo Miranda dos, Rodrigo Covre Vieira, Louise de Souza Canto Covre, Milena Cristina Martins da Silva, Thiago de Matos Bezerra, Geraldo Mariano Moraes de Macedo, Edna Aoba Yassui Ishikawa, Karla Valéria Batista Lima, Maísa Silva de Sousa, and Rodrigo Vellasco Duarte Silvestre. 2026. "High Burden of Chlamydia trachomatis and Human Papillomavirus Infections in Low-Income Female University Students from Public Schools in the Brazilian Amazon" Microorganisms 14, no. 6: 1176. https://doi.org/10.3390/microorganisms14061176

APA Style

Santos, L. M. d., Vieira, R. C., de Souza Canto Covre, L., da Silva, M. C. M., Bezerra, T. d. M., de Macedo, G. M. M., Ishikawa, E. A. Y., Lima, K. V. B., de Sousa, M. S., & Silvestre, R. V. D. (2026). High Burden of Chlamydia trachomatis and Human Papillomavirus Infections in Low-Income Female University Students from Public Schools in the Brazilian Amazon. Microorganisms, 14(6), 1176. https://doi.org/10.3390/microorganisms14061176

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