Meta-Analysis of The Prevalence of Genital Infections Among Hiv Carriers and Uninfected Women
REVIEW ARTICLE

Meta-Analysis of The Prevalence of Genital Infections Among Hiv Carriers and Uninfected Women

Ana Paula Ferreira Costa1 , * Open Modal Marcos Gonzaga dos Santos2 Ayane Cristine Alves Sarmento3 Pedro Henrique Alcântara da Silva4 Guilherme Maranhão Chaves3 Janaina Cristiana de Oliveira Crispim2 Ana Katherine Gonçalves4 Ricardo Ney Oliveira Cobucci5
Authors Info & Affiliations
The Open AIDS Journal • 30 Oct 2018 • REVIEW ARTICLE • DOI: 10.2174/1874613601812010136

Abstract

Background & Aim:

The risk factors in acquiring genital co-infections associated with HIV infection still present many questions. We conducted a systematic review and meta-analysis to compare the prevalence of genital infection among HIV-infected and uninfected women.

Methods:

We searched PubMed, Web of Science, Scopus and Scielo for the relevant studies up until October 2017. Data were collected from the included studies and methodologically assessed. Odds ratios (OR) and 95% confidence intervals (CI) were pooled using fixed or random-effects models.

Results:

Thirty-six articles involving 23,863 women with retroviruses were included. HIV-infected women were significantly more diagnosed with the following genital infections: Herpes simplex virus type 2 (HSV-2) (OR 3.70; 95% CI: 2.42–5.65), Neisseria gonorrhoeae (GC) (OR 4.18; 95% CI: 2.15-8.13), Chlamydia trachomatis (CT) (OR 2.25; 95% CI: 1.20-4.23) and Human papillomavirus (HPV) (OR 3.99, 95% CI: 3.35-4.75). There was no significant difference in the prevalence of bacterial vaginosis (OR 1.09; 95% CI: 0.91-1.30), Candida sp. (OR 1.51; 95% CI: 0.71-3.25), Treponema pallidum (OR 1.56; 95% CI: 1.00-2.45) and Trichomonas vaginalis (OR 1.00; 95% CI: 0.47-2.15).

Conclusion:

The prevalence of HPV, HSV-2, GC and CT genital infection was significantly higher among HIV-positive women.

Keywords: HIV, Microbiota, Reproductive Tract Infections, Sexually Transmitted Diseases, Genital Infections, Uninfacted Women.

1. INTRODUCTION

The microflora of healthy vaginal mucosa is typically dominated by the Lactobacillus species, which serve as an important natural barrier against infection [1]. Clinical studies have shown an association between the presence of lactobacillus and a decrease in the prevalence of gonorrhea, bacterial vaginosis and Human Immunodeficiency Virus (HIV) infection [2, 3].

Recently, many epidemiological studies have highlighted the increase in the prevalence of genital infection in certain sub-populations of women. There have been fewer publications addressing the changing epidemiology of Sexually Transmitted Diseases (STD) among women, and these publications have demonstrated that the risk of STD has significantly increased among HIV-positive women [4].

Sexually transmitted infections are a major public health concern in many developing countries. Women are more likely to bear the burden of these infections but less likely to seek medical treatment. The World Health Organization (WHO) estimates that globally, there are about 340 million new cases of curable STDs (Chlamydia, gonorrhea, syphilis and trichomoniasis) each year [5].

There are gaps in the knowledge of how certain STD or microbiota imbalances can facilitate the HIV infection. It is well accepted that Trichomonas vaginalis infection and bacterial vaginosis can lead to changes in the innate and adaptive immune response in women’s lower genital tract through the presence of microbial products, induction of proinflammatory cytokines, cell recruitment and loss of epithelium integrity. These alterations are associated with an increase in HIV infection rates related to these pathogens [6, 7].

On the other hand, the knowledge regarding risk factors for acquiring genital co-infections associated with HIV infection is still incomplete and many associations are still considered controversial, as is the case for the association of vulvovaginal candidiasis with HIV. Women with recurrent candidiasis are often recommended to test for HIV, however, some authors maintain that there is no direct association between candidiasis and HIV infection and that the clinical manifestation is no different from that observed in HIV uninfected women [8, 9].

The aim of this meta-analysis is to compare the prevalence of some genital infections among HIV carriers and uninfected women.

2. MATERIALS AND METHODS

2.1. Study Design

This meta-analysis was designed and reported according to the modified Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [10]. Since this study was based on previously published studies, no ethical approval and patient consent was required.

2.2. Search Strategy

The literature searches were conducted in the following electronic databases: PubMed, Web of Science, Scopus and Scielo from January 1991 to October 2017. The following MeSH terms and keywords were used: [HIV] and [HIV infection] and [Sexually Transmitted Diseases] and [microbiome] or [vaginal microbiome] or [cervicovaginal microbiota] or [vaginal diseases] or [vaginitis] and [symptoms] and [women]. No language restrictions were applied and four independent researchers (APFC, ACAS, PHAS and MGS) performed this search. The flowchart of this study is shown in Fig. (1).

All potentially relevant publications were then evaluated by three individuals (APFC, MGS and RNOC) and were included in this review if they addressed any of the following criteria: (1) Cross-sectional and cohort studies involving only non-pregnant women and (2) Comparing prevalence of genital infections among women with and without HIV. Publications were excluded if they were case reports, reviews, included men and did not include original data. Reference lists of included studies were manually screened to identify other relevant publications. Disagreements were resolved by means of mutual consensus.

Fig. (1). Flow diagram of the search process.

2.3. Data Extraction

Table 1 lists the studies included in this review. Study characteristics (author, publication date, study design, period, types of microorganisms and diagnosis tests used) and study population (study location, number and age range of participants) were extracted from all included studies. We identified peer-reviewed publications that included the following criteria: population: women diagnosed with HIV; intervention: diagnostic tests to assess the presence of genital infection; control: women not infected with HIV; outcome: prevalence of genital infection. We only included Cross-sectional and cohort studies which covered all the points of the PICO strategy. When duplicate publications or secondary publications with overlapping patient populations were detected, the authors were contacted to collect non-overlapping data for inclusion in the meta-analysis. Three reviewers (JCOC, AKG and GMC) extracted the data from all articles and any disagreement was resolved by consensus.

Table 1.
Description of the characteristics of included studies.
Author, Year Country Design of Study Types of Microorganisms Methodology Follow-up Age Range (y) Sample Size
Reference
Vermund, et al. 1991 [19] USA Cross-sectional HPV PCR - 23-58 97
Miott, et al. 1996 [21] Malawi Cross-sectional HPV PCR 1 year - 284
Chiasson, et al. 1997 [47] USA Cross-sectional HPV PCR - >18 771
Uberti-foppa, et al. 1998 [23] Italy Cross-sectional HPV PCR 1 year and 10 months 21-64 268
Cu-uvin, et al. 1999 [2] USA Cohort BV Clinical examination 1 year and 9 months 16-55 1.31
HPV PCR
Candida sp. Culture
N. gonorrhoeae Serology
Treponema pallidum Culture
T. vaginalis Serology
Chlamydia trachomatis  
Warren, et al. 2001 [39] USA Cohort Gardnerella sp. Gram 1 year and 9 months 16-55 1.31
BV
Conley, et al. 2002 [22] USA Cohort HPV PCR 6 years and 11 months 16-35 925
Branca, et al. 2003 [26] Italy Cohort HPV PCR 2 years 17-45 142
Viscidi, et al. 2003 [27] USA Cohort HPV PCR 1 year and 9 months 16-55 2.559
Viscidi, et al. 2003b [28] USA cohort HPV PCR 1 year and 9 months 16-55 2.524
Ohmit, et al. 2003 [44] USA Cohort Candida sp. Culture 1 year and 9 months 16-55 1.31
Harris, et al. 2005 [29] USA Cohort HPV PCR 1 year 34-36 1.198
Watts, et al. 2005 [24] USA Cohort BV Nugent criteria 1 year and 1 month - 2.229
HPV PCR
T. vaginalis Fresh examination
Watts, et al. 2006 [25]. USA and Hawaii Cohort BV Gram 1 year and 1 month - 2.652
HPV PCR
T. vaginalis Fresh examination
Didelot-rousseau, et al. 2006 [31]. Bobo-Dioulasso Cross-sectional HPV PCR - 16-54 379
Ng´andwe, et al. 2007 [32] Zambia Cohort HPV PCR 1 year and 1 month 15-38 70
sha 2007 [16] USA Cohort BV Nugent criteria 1 years and 1 month - 2.628
Candida sp. Smear with potassium hydroxide (KOH)
T. vaginalis Fresh examination
Singh, et al. 2009 [33] Rwanda Cohort HPV PCR 6 months >25 936
Desruisseau, et al. 2010 [35] Camaroon Cross-sectional HPV PCR 10 years and 11 months >18 65
Djigma, et al. 2011 [34] Burkina Faso Cohort Mycoplasma sp. PCR 6 months 27-45 451
Candida sp. Culture
N. gonorrhoeae  
Nowark, et al. 2011 [45]. Zimbabue Cohort HSV-2 ELISA 4 years and 2 months 28-35 641
BV AMSEL CRITERIA
HPV PCR
N. gonorrhoeae  
Chlamydia trachomatis  
Gallo, et al. 2011 [40] USA Cohort BV Nugent criteria 2 years 16-55 1364
Oliveira, et al. 2011 [17] Brazil Cross- sectional Candida sp. Culture 1 year >18 140
Chiduo, et al. 2012 [30] Tanzania Cohort Candida sp. Gram 2 years >18 205
Treponema pallidum Serology
T. vaginalis Fresh examination PCR
Chlamydia trachomatis  
Blitz, et al. 2013 [36] Canada Cohort HPV PCR 9 years 15-44 923
Hu, et al. 2013 [18] USA Cohort Candida sp. Culture                  4 years and 5 months >18 24
Apalata, et al. 2014 [20] South Africa Cohort HSV-2 PCR 7 months >18 198
Mycoplasma sp. Culture
Candida sp. PCR
N. gonorrhoeae  
T. vaginalis  
Chlamydia trachomatis  
Benning, et al. 2014 [41] USA and Rwandan Cohort N. gonorrhoeae Sequencing 1 years and 10 months 33-51 86
Mackelprang, et al. 2015 [43] USA Cross-sectional BV Nugent criteria - - 372
Masson, et al. 2015 [42] South Africa Cross-sectional HSV-2 ELISA - 18-59 265
BV Nugent criteria
Mycoplasma sp. PCR
N. gonorrhoeae Quick test
Treponema pallidum PCR
T. vaginalis  
Chlamydia trachomatis  
Alczuk, et al. 2015 [15] Unganda Cohort Candida sp. Culture 4 years and 2 months 18-35 641
Massad, et al. 2016 [37] USA Cohort HPV PCR 8 years >18 3438
Reimers, et al. 2016 [38] USA Cohort HPV PCR 8 years >18 64
Kriek, et al. 2016 [46] South Africa Cohort HPV PCR 6 months 28-42 165
Mycoplasma sp.
N. gonorrhoeae
T. vaginalis
Chlamydia trachomatis
Alcaide, et al. 2016 [14] USA Cross-sectional BV Nugent criteria 8 months 18-45 34

2.4. Risk of Bias Assessments

The Cochrane Collaboration tool for assessing the risk of bias was applied to evaluate the following criteria: The adequate sequence generation, allocation concealment, blinding, incomplete outcome data, selective reporting and other risks of bias [11]. Two authors (ACAS and PHAS) assessed each original study and the quality of the accurate information of the studies was demonstrated in Table 2. Each of the previously cited criteria received one of the following classifications: “low risk of bias”, “high risk of bias”, or “unclear risk of bias”. Disagreements were resolved by consulting a third author (RNOC).

2.5. Data Analysis

Dichotomous data from each of the eligible studies were combined for meta-analysis using the Mantel/Haenszel model. Results were expressed as Odds Ratios (OR) with 95% Confidence Intervals (CI). Fixed-effects or random-effects models were chosen depending on whether there was an absence or presence of heterogeneity between studies. Statistical heterogeneity was assessed by the I2 statistic (<25%, no heterogeneity; 25%–50%, moderate heterogeneity; and >50%, strong heterogeneity). When a significant heterogeneity existed across the included studies (I2 > 50%), a random-effects model was used for the analysis; otherwise, the fixed-effects model was used [12, 13]. Meta-regression was conducted to investigate the potential heterogeneity. In addition, we used the Egger funnel plot to assess possible publication bias (12). All tests were performed using Review Manager (RevMan version 5.3.0) software and two-sided p value < 0.05 was considered statistically significant.

Table 2.
Quality assessment of the included studies.
Study/Year
Reference		 Random sequence generation Allocation concealment Blinding of participants and personnel Blinding of outcome assessment Incomplete outcome data Selective reporting Other bias
Vermund 1991 [19]
Miott 1996 [21]
Chiasson 1997 [47]
Uberti-Foppa 1998 [23]
Cu-Uvin 1999 [2]
Warren 2001 [39]
Conley 2002 [22]
Branca 2003 [26]
Viscidi 2003 [27]
Viscidi 2003b [28]
Ohmit 2003 [44]
Harris 2005 [29]
Watts 2005 [24]
Watts 2006 [25]
Didelot-Rousseau 2006 [31]
Ng´andwe 2007 [32]
Sha 2007 [16]
Singh 2009 [33]
Desruisseau 2010 [35]
Djigma 2011 [34]
Nowark 2011 [45]
Gallo 2011 [40]
Oliveira 2011 [17]
Chiduo 2012 [30]
Blitz 2013 [36]
Hu 2013 [18]
Apalata 2014 [20]
Benning 2014 [41]
Mackelprang 2015 [43]
Masson 2015 [42]
Alczuk 2015 [15]
Massad 2016 [37]
Reimers 2016 [38]
Kriek 2016 [46]
Alcaide 2016 [14]
:High risk of bias: Unclear risk of bias: Low risk of bias

3. RESULTS

A total of 36 relevant published articles were included for meta-analysis, involving 23,863 HIV-infected women [2, 14-47] Table 1. Among those infected by HIV there was a significantly higher prevalence of genital infection by certain microorganisms compared to uninfected women.

3.1. Subgroup Analysis

Subgroup analysis was carried out for microorganisms that cause STD (Fig. 2) and for those found in the microbiota of the female genital tract (Fig. 3), which cause genital infection when there is an imbalance of the vaginal microflora.

3.1.1. Human Papillomavirus (HPV)

The prevalence of HPV (OR 3.99, 95% CI: 3.35-4.75) in the reproductive tract was significantly higher in HIV-infected women than in similarly aged control women.

3.1.2. Herpes Simplex Virus Type 2 (HSV-2)

Similarly, HSV-2 (OR 3.70; 95% CI 2.42-5.65) genital infection was more prevalent among retrovirus carriers.

3.1.3. Neisseria Gonorrhoeae (GC)

The diagnosis of GC (OR 4.18; 95% CI 2.15-8.13) was also significantly higher among HIV-infected women.

3.1.4. Chlamydia Trachomatis (CT)

Vaginal and cervical CT infections (OR 2.25; 95% CI 1.20-4.23) were significantly more prevalent among those infected with HIV.

3.1.5. Treponema Pallidum (TP)

Among the Sexually Transmitted Infections (STI) investigated in the reproductive tract of women of both groups, there was not a higher prevalence of TP infection (OR 1.56; 95% CI 1.00-2.45), the causative agent of syphilis.

3.1.6. Trichomonas Vaginalis (TV)

TV (OR 1.00; 95% CI 0.47-2.15) was the other microorganism transmitted through sexual contact whose prevalence was no different between the groups.

3.1.7. Bacterial Vaginosis (BV)

The prevalence of microorganisms causing BV (Gardnerella vaginalis, Mycoplasma sp., etc.), not considered a STI, was not significantly different between the groups (OR 1.09; 95% CI 0.91-1.30).

3.1.8. Candida sp.

Finally, there was no significant difference in fungal infection by different Candida species in the genital tract of women in both groups (OR 1.51; 95% CI 0.71-3.25).

3.1.9. Publication Bias

Potential publication bias was not presented according to the funnel plots, which are shown in (Figs. 2 and 3).

Fig. (2). Forest and funnel plots of sexually transmitted diseases.
Fig. (3). Forest and funnel plots of genital infection.

3.1.10. Meta-Regression

Using meta-regression there was little evidence of heterogeneity between any of these subgroups (p >0.05 by meta-regression).

4. DISCUSSION

This meta-analysis found that HIV carriers are more likely to be diagnosed with certain genital infections than women not infected with the virus. Subgroup analysis showed that the prevalence of most STIs is significantly higher among women with HIV, while infections caused by microorganisms of the vaginal microbiome are no longer prevalent in this group.

HIV can affect the immunological host response, resulting in an increased susceptibility to STIs. In women, this association was observed mainly in the presence of microorganisms causing intraepithelial lesions as well as cervicitis, which disturbs the epithelial barrier, causing local inflammation and increases the viral load of the genital tract [3, 48].

In this meta-analysis, the prevalence of STI was reported in all the analyzed studies [2, 14-47]. The most reported infections were HPV, Candida sp., BV, T. pallidum, T. vaginalis, N. gonorrhoeae, C. trachomatis and HSV-2. The susceptibility to STI may increase because of the negative effects of HIV infection on the immunity system, which is often unable to mount a protective response against sexually transmitted pathogens [49]. In line with this, HIV positive women were significantly more infected by HPV, HSV-2, GC and CT, compared to women not infected by the virus.

HPV genital infection can lead to cervical cancer. Co-infection with HIV increases the burden of HPV infection [50]. HIV-positive women are more vulnerable to HPV infection and have a lower propensity to eliminate this virus, increasing the risk of developing lesions and cancer [47]. These women, especially those with lower CD4 cell counts, have a higher prevalence of anal and cervical HPV infection and HPV cancers [51]. HPV detection by PCR has significantly increased in HIV positive women, as in a previous meta-analysis that indicated a higher prevalence of high-risk type HPV-16 in HIV infected women, and a higher incidence of multiple HPV infection in this group, with a consequent higher rate of high grade lesions [50, 52, 53].

Bacterial vaginosis and Trichomonas vaginalis infection are very common and are associated with an increased risk of sexual transmission of HIV. Previous studies [54-59] indicated that BV was associated with an increased risk of HIV transmission, probably as a result from an imbalance in the immune response, loss of epithelial integrity and an increase in HIV shedding, especially when associated with TV infection. It was previously reported that HIV infected women with controlled viral load might be less likely to have BV, possibly because those women are more likely to abstain from sex or to use condoms [60]. Bacterial vaginosis data was determined by the Nugent criteria in all selected studies and there was no significant difference in the prevalence among the groups. Moreover, despite the role played by T. vaginalis in HIV transmission, laboratory detection of the parasite was not more frequent in HIV positive women, suggesting that the immunological response against this infection is not impaired by the HIV presence.

The frequency of vulvovaginal candidiasis (VVC) caused by Candida species, such as Candida albicans, Candida tropicalis, Candida glabrata, and Candida krusei is increasing, especially in HIV-infected women [61]. However, the prevalence of VVC was not higher among HIV-infected women in this meta-analysis, in agreement with previous reports [20], which indicate that the HIV load is not associated with an increased risk of symptomatic VVC.

Sexually transmitted pathogens, such as Neisseria gonorrhoeae (GC) and Chlamydia trachomatis (CT) are associated with increased HIV particles in genital secretions. During chronic HIV infection, GC infection was associated with a transient increase in plasma viremia and cytokines, such as IL-4 and IL-10, and a decrease in CD4+ T cell counts [62]. A previous study from Brazil reported higher rates of GC among HIV-infected women [63]. Moreover, it was previously reported that there was a higher frequency in antibiotic-resistant strains in patients co-infected with GC and HIV, possibly a consequence of repeated treatments [64]. Likewise, studies indicate that genital CT infection is more prevalent in women with the virus, corroborating the findings of this study [65, 66].

Syphilis is an emerging STD that has been growing in recent years especially among people with HIV. Syphilis and HIV appear to be the most commonly reported STDs [67]. Some studies have shown that the prevalence of syphilis among women is increasing worldwide [68]. In this meta-analysis, the prevalence of T. pallidum infection was no different between the groups, in agreement with the findings of previous studies [69, 70].

The decrease in the host's innate or adaptive immune response results in infectious clinical conditions, which may be persistent or disseminated. Persistent HSV-2 is a common presentation of HIV type 1 (HIV-1) advanced infection; low CD4 counts and high viral load facilitate the emergence of HSV-2 infections [71-74]. This fact justifies the higher prevalence of the herpes virus in the genital tract of women with HIV, as verified in this study.

Some limitations in our study should be addressed. First, as with any systematic review and meta-analysis, there was the unavoidable heterogeneity among different studies, which could distort the combined estimates. Secondly, another potential limitation of the study was the various methods used to diagnose STI among the different studies. Thirdly, all the included studies were observational studies, which can introduce recall bias or selection bias. Finally, our study did not address the issues related to the participants’ disease history at baseline, since the studies included had no information regarding sexual behavior, CD4 and CD8 levels, and the severity of HIV infection in HIV-infected women, which has been shown to influence the risk of genital infection. Furthermore, one possibility is that women living with HIV who have been evaluated for the prevalence of STD in studies conducted after the introduction of Antiretroviral Therapy (ART) have less infection than those assessed prior to therapy. However, the purpose of the meta-analysis was to compare the prevalence of infections among HIV-infected and non-HIV-infected women, and because most of the included studies are cross-sectional, we cannot establish the relationship between ART use and the decrease or increase in infection diagnosis.

CONCLUSION

This meta-analysis demonstrated that individuals with HIV had a significantly increased prevalence of syphilis, HPV, HSV-2, N. gonorrhoeae and C. trachomatis. However, owing to the inherent limitations of the included studies, further high-quality, prospective, and multicentered studies are needed to confirm our result.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

1
Damelin LH, Paximadis M, Mavri-Damelin D, Birkhead M, Lewis DA, Tiemessen CT. Identification of predominant culturable vaginal Lactobacillus species and associated bacteriophages from women with and without vaginal discharge syndrome in south africa. J Med Microbiol 2011; 60(Pt 2): 180-3.
2
Cu-Uvin S, Hogan JW, Warren D, et al. Prevalence of lower genital tract infections among human immunodeficiency virus (HIV)-seropositive and high-risk HIV-seronegative women. Clin Infect Dis 1999; 29(5): 1145-50.
3
Tanton C, Weiss HA, Le Goff J, et al. Correlates of HIV-1 genital shedding in Tanzanian women. PLoS One 2011; 1;6(3): e17480..
4
Zuma K, Lurie MN, Williams BG, Mkaya-Mwamburi D, Garnett GP, Sturm AW. Risk factors of sexually transmitted infections among migrant and non-migrant sexual partnerships from rural south africa. Epidemiol Infect 2005; 133(3): 421-8.
5
Lewis DA. HIV/sexually transmitted infection epidemiology, management and control in the IUSTI Africa region: Focus on sub-Saharan Africa. Sex Transm Infect 2011; 87(Suppl. 2): ii10-3.
6
Kissinger P, Adamski A. Trichomoniasis and HIV interactions: A review. Sex Transm Infect 2013; 89(6): 426-33.
7
Mirmonsef P, Krass L, Landay A, Spear GT. The role of bacterial vaginosis and trichomonas in HIV transmission across the female genital tract. Curr HIV Res 2012; 10(3): 202-10.
8
Duerr A, Heilig CM, Meikle SF, et al. Incident and persistent vulvovaginal candidiasis among human immunodeficiency virus-infected women: Risk factors and severity. Obstet Gynecol 2003; 101(3): 548-56.
9
Sobel JD. Vulvovaginal candidiasis: A comparison of HIV-positive and -negative women. Int J STD AIDS 2002; 13(6): 358-62.
10
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 2009; 6(7): e1000097.
11
Higgins J, Altman D, Sterne J. Chapter 8: Assessing risk of bias in included studies. Cochrane Handbook for systematic reviews of interventions Version 5.1. 0 (updated March 2011). The Cochrane Collaboration 2011.
12
Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327(7414): 557-60.
13
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7(3): 177-88.
14
Alcaide ML, Strbo N, Romero L, et al. Bacterial vaginosis is associated with loss of gamma delta T cells in the female reproductive tract in women in the miami Women Interagency HIV Study (WIHS): A cross sectional study. PLoS One 2016; 14;11(4): e0153045..
15
Alczuk SdeS, Bonfim-Mendonça PdeS, Rocha-Brischiliari SC, et al. Effect of highly active antiretroviral therapy on vaginal candida spp. isolation in HIV-infected compared to HIV-uninfected women. Rev Inst Med Trop São Paulo 2015; 57(2): 169-74.
16
Sha BE, Gawel SH, Hershow RC, et al. Analysis of standard methods for diagnosing vaginitis: HIV infection does not complicate the diagnosis of vaginitis. J Low Genit Tract Dis 2007; 11(4): 240-50.
17
Oliveira PM, Mascarenhas RE, Lacroix C, et al. Candida species isolated from the vaginal mucosa of HIV-infected women in salvador, bahia, brazil. Braz J Infect Dis 2011; 15(3): 239-44.
18
Hu H, Merenstein DJ, Wang C, et al. Impact of eating probiotic yogurt on colonization by candida species of the oral and vaginal mucosa in HIV-infected and HIV-uninfected women. Mycopathologia 2013; 176(3-4): 175-81.
19
Vermund SH, Kelley KF, Klein RS, et al. High risk of human papillomavirus infection and cervical squamous intraepithelial lesions among women with symptomatic human immunodeficiency virus infection. Am J Obstet Gynecol 1991; 165(2): 392-400.
20
Apalata T, Carr WH, Longo-Mbenza B, Sturm WA, Moodley P. Association between symptomatic vulvovaginal candidiasis and HIV RNA levels in plasma and genital secretions among women on HAART. South Afr J HIV Med 2014; 15(2): 57-64.
21
Motti PG, Dallabetta GA, Daniel RW, et al. Cervical abnormalities, human papillomavirus, and human immunodeficiency virus infections in women in Malawi. J Infect Dis 1996; 173(3): 714-7.
22
Conley LJ, Ellerbrock TV, Bush TJ, Chiasson MA, Sawo D, Wright TC. HIV-1 infection and risk of vulvovaginal and perianal condylomata acuminata and intraepithelial neoplasia: A prospective cohort study. Lancet 2002; 12;359(9301): 108-3.
23
Uberti-Foppa C, Origoni M, Maillard M, et al. Evaluation of the detection of human papillomavirus genotypes in cervical specimens by hybrid capture as screening for precancerous lesions in HIV-positive women. J Med Virol 1998; 56(2): 133-7.
24
Watts DH, Fazzari M, Minkoff H, et al. Effects of bacterial vaginosis and other genital infections on the natural history of human papillomavirus infection in HIV-1-infected and high-risk HIV-1-uninfected women. J Infect Dis 2005; 1;191(7): 1129-39.
25
Watts DH, Springer G, Minkoff H, et al. The occurrence of vaginal infections among HIV-infected and high-risk HIV-uninfected women: Longitudinal findings of the women's interagency HIV study. J Acquir Immune Defic Syndr 2006; 1;43(2): 161-8.
26
Branca M, Garbuglia AR, Benedetto A, et al. Factors predicting the persistence of genital human papillomavirus infections and PAP smear abnormality in HIV-positive and HIV-negative women during prospective follow-up. Int J STD AIDS 2003; 14(6): 417-25.
27
Viscidi RP, Ahdieh-Grant L, Schneider MF, et al. Serum immunoglobulin a response to human papillomavirus type 16 virus-like particles in human immunodeficiency virus (HIV)-positive and high-risk HIV-negative women. J Infect Dis 2003; 15;188(12): 1834-44.
28
Viscidi RP, Ahdieh-Grant L, Clayman B, et al. Serum immunoglobulin G response to human papillomavirus type 16 virus-like particles in human immunodeficiency virus (HIV)-positive and risk-matched HIV-negative women. J Infect Dis 2003; 15;187(2): 194-205.
29
Harris TG, Burk RD, Palefsky JM, et al. Incidence of cervical squamous intraepithelial lesions associated with HIV serostatus, CD4 cell counts, and human papillomavirus test results. JAMA. 2005; 23;293(12): 1471-6.
30
Chiduo M, Theilgaard ZP, Bakari V, et al. Prevalence of sexually transmitted infections among women attending antenatal clinics in Tanga, north eastern Tanzania. Int J STD AIDS 2012; 23(5): 325-9.
31
Didelot-Rousseau MN, Nagot N, Costes-Martineau V, et al. Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-1 infection in Burkina Faso. Br J Cancer 2006; 7(95(5)): 355-62.
32
Ng'andwe C, Lowe JJ, Richards PJ, Hause L, Wood C, Angeletti PC. The distribution of sexually-transmitted Human Papillomaviruses in HIV positive and negative patients in Zambia, Africa. BMC Infect Dis 2007; 16: 7-77.
33
Singh DK, Anastos K, Hoover DR, et al. Human papillomavirus infection and cervical cytology in HIV-infected and HIV-uninfected Rwandan women. J Infect Dis 2009; 15;199(12): 1851-61.
34
Djigma FW, Ouédraogo C, Karou DS, et al. Prevalence and genotype characterization of human papillomaviruses among HIV-seropositive in ouagadougou, burkina faso. Acta Trop 2011; 117(3): 202-6.
35
Desruisseau AJ, Schmidt-Grimminger D, Welty E. Epidemiology of HPV in HIV-positive and HIV-negative fertile women in Cameroon, west africa. Infect Dis Obstet Gynecol 2009; 2009: 810596.
36
Blitz S, Baxter J, Raboud J, et al. Canadian Women's HIV Study Group. Evaluation of HIV and highly active antiretroviral therapy on the natural history of human papillomavirus infection and cervical cytopathologic findings in HIV-positive and high-risk HIV-negative women. J Infect Dis 2013; 1;208(3): 454-62.
37
Massad LS, Xie X, Burk RD, et al. Association of cervical precancer with human papillomavirus types other than 16 among HIV co-infected women. Am J Obstet Gynecol 2016; 214(3): 354.e1-6.
38
Reimers LL, Mehta SD, Massad LS, et al. The cervicovaginal microbiota and its associations with human papillomavirus detection in HIV-infected and HIV-uninfected women. J Infect Dis 2016; 1;214(9): 1361-9.
39
Warren D, Klein RS, Sobel J, et al. HIV Epidemiology Research Study Group. A multicenter study of bacterial vaginosis in women with or at risk for human immunodeficiency virus infection. Infect Dis Obstet Gynecol 2001; 9(3): 133-41.
40
Gallo MF, Jamieson DJ, Cu-Uvin S, Rompalo A, Klein RS, Sobel JD. Accuracy of clinical diagnosis of bacterial vaginosis by human immunodeficiency virus infection status. Sex Transm Dis 2011; 38(4): 270-4.
41
Benning L, Golub ET, Anastos K, et al. Comparison of lower genital tract microbiota in HIV-infected and uninfected women from Rwanda and the US. PLoS One 2014; 9;9(5): e96844.
42
Masson L, Passmore JA, Liebenberg LJ, et al. Genital inflammation and the risk of HIV acquisition in women. Clin Infect Dis 2015; 15;61(2): 260-9.
43
Mackelprang RD, Scoville CW, Cohen CR, et al. Toll-like receptor gene variants and bacterial vaginosis among HIV-1 infected and uninfected African women. Genes Immun 2015; 16(5): 362-5.
44
Ohmit SE, Sobel JD, Schuman P, et al. Longitudinal study of mucosal Candida species colonization and candidiasis among human immunodeficiency virus (HIV)-seropositive and at-risk HIV-seronegative women. J Infect Dis 2003; 188(1): 118-27.
45
Nowak RG, Gravitt PE, Morrison CS, et al. Increases in human papillomavirus detection during early HIV infection among women in Zimbabwe. J Infect Dis 2011; 15;203(8): 1182-91.
46
Kriek JM, Jaumdally SZ, Masson L, et al. Female genital tract inflammation, HIV co-infection and persistent mucosal Human Papillomavirus (HPV) infections. Virology 2016; 493: 247-54.
47
Chiasson MA, Ellerbrock TV, Bush TJ, Sun XW, Wright TC Jr. Increased prevalence of vulvovaginal condyloma and vulvar intraepithelial neoplasia in women infected with the human immunodeficiency virus. Obstet Gynecol 1997; 89(5 Pt 1): 690-4.
48
Wasserheit, J. Epidemiological synergy.. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 61-77.
49
McCoy SI, Eron JJ, Kuruc JD, et al. Sexually transmitted infections among patients with acute HIV in north carolina. Sex Transm Dis 2009; 36(6): 372-4.
50
Clifford GM, Tully S, Franceschi S. Carcinogenicity of Human Papillomavirus (HPV) types in HIV-positive women: A meta-analysis from HPV infection to cervical cancer. Clin Infect Dis 2017; 64(9): 1228-35.
51
Ahdieh L, Klein RS, Burk R, et al. Prevalence, incidence, and type-specific persistence of human papillomavirus in human immunodeficiency virus (HIV)-positive and HIV-negative women. J Infect Dis 2001; 64(9): 1228-35.
52
Clifford GM, de Vuyst H, Tenet V, Plummer M, Tully S, Franceschi S. Effect of HIV infection on human papillomavirus types causing invasive cervical cancer in africa. J Acquir Immune Defic Syndr 2016; 1;73(3): 332-9.
53
Ceccato Junior BP, Lopes APC, Nascimento LF, Novaes LM, Melo VH. Prevalência de infecção cervical por papilomavírus humano e neoplasia intraepitelial cervical em mulheres HIV-positivas e negativas. Rev Bras Ginecol Obstet 2015; 37(4): 178-85. [Portuguese].
54
Atashili J, Poole C, Ndumbe PM, Adimora AA, Smith JS. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 2008; 31;22(12): 1493-501.
55
Cohen CR, Lingappa JR, Baeten JM, et al. Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: A prospective cohort analysis among African couples. PLoS Med 2012; 9(6): e1001251.
56
Myer L, Denny L, Telerant R, Souza Md, Wright TC Jr, Kuhn L. Bacterial vaginosis and susceptibility to HIV infection in south african women: A nested case-control study. J Infect Dis 2005; 192(8): 1372-80.
57
Kissinger P, Adamski A. Trichomoniasis and HIV interactions: A review. Sex Transm Infect 2013; 89(6): 426-33.
58
Mirmonsef P, Krass L, Landay A, Spear GT. The role of bacterial vaginosis and trichomonas in HIV transmission across the female genital tract. Curr HIV Res 2012; 10(3): 202-10.
59
Fastring DR, Amedee A, Gatski M, et al. Co-occurrence of Trichomonas vaginalis and bacterial vaginosis and vaginal shedding of HIV-1 RNA. Sex Transm Dis 2014; 41(3): 173-9.
60
French AL, Adeyemi OM, Agniel DM, et al. The association of HIV status with bacterial vaginosis and vitamin D in the United States. J Womens Health (Larchmt) 2011; 20(10): 1497-503.
61
Sobel JD, Ohmit SE, Schuman P, et al. The evolution of Candida species and fluconazole susceptibility among oral and vaginal isolates recovered from human immunodeficiency virus (HIV)-seropositive and at-risk HIV-seronegative women. J Infect Dis 2001; 183(2): 286-93.
62
Page KR, Moore RD, Wilgus B, Gindi R, Erbelding EJ. Neisseria gonorrhoeae and Chlamydia trachomatis among human immunodeficiency virus-infected women. Sex Transm Dis 2008; 35(10): 859-61.
63
Miranda AE, Silveira MF, Travassos AG, et al. Prevalence of chlamydia trachomatis and Neisseria gonorrhea and associated factors among women living with Human Immunodeficiency Virus in Brazil: A multicenter study. Braz J Infect Dis 2017; 21(4): 402-7.
64
Mir BA, Sirwar SB, Vijayaraghavan R. Prevalence and antibiotic susceptibility of neisseria gonorrhoeae in HIV positive and hiv negative cases at a tertiary care hospital. Indian J Microbiol Res 2016; 3(2): 213-8.
65
Buckner LR, Amedee AM, Albritton HL, et al. Chlamydia trachomatis infection of endocervical epithelial cells enhances early HIV transmission events. PLoS One 2016; 11(1): e0146663.
66
Guthrie BL, Kiarie JN, Morrison S, et al. Sexually transmitted infections among HIV-1-discordant couples. PLoS One 2009; 4(12): e8276.
67
Niama RF, Loukabou Bongolo NC, Bayonne Kombo ES, et al. Syphilis and HIV infections among pregnant women attending antenatal clinics in republic of congo. Pan Afr Med J 2017; 7(12): 28-8.
68
Newman L, Rowley J, Vander Hoorn S, et al. Global estimates of the Prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One 2015 Dec 8; 10(12): e0143304.
69
Hu QH, Xu JJ, Zou HC, et al. Risk factors associated with prevalent and incident syphilis among an HIV-infected cohort in Northeast China. BMC Infect Dis 2014; 14(1): 658.
70
Manyahi J, Jullu BS, Abuya MI, et al. Prevalence of HIV and syphilis infections among pregnant women attending antenatal clinics in tanzania, 2011. BMC Public Health 2015; 22: 15-501.
71
Posavad CM, Wald A, Kuntz S, et al. Frequent reactivation of herpes simplex virus among HIV-1-infected patients treated with highly active antiretroviral therapy. J Infect Dis 2004 Aug 15; 190(4): 693-6.
72
Cheng RG, Nixon DF, Mayaud P. Herpes simplex virus and HIV-1: Deciphering viral synergy. Lancet Infect Dis 2009; 9(2): 74-5.
73
Barnabas RV, Celum C. Infectious co-factors in HIV-1 transmission herpes simplex virus type-2 and HIV-1: new insights and interventions. Curr HIV Res 2012; 10(3): 228-37.
74
Looker KJ, Elmes JAR, Gottlieb SL, et al. Effect of HSV-2 infection on subsequent HIV acquisition: An updated systematic review and meta-analysis. Lancet Infect Dis 2017; 17(12): 1303-16.