Skip to main content
NCBI home page
Wiley Open Access Collection logoLink to Wiley Open Access Collection
. 2025 Apr 2;97(4):e70274. doi: 10.1002/jmv.70274

The Burden of HPV Infections and HPV‐Related Diseases Among People With HIV: A Systematic Literature Review

Bekana K Tadese 1,✉, Xuedan You 1, Tidiane Ndao 1, Joseph E Tota 1, Ya‐Ting Chen 1, Alisa Chowdhary 2, Jia Pan 2, Ana C Costa 2, Nelly Mugo 3
PMCID: PMC11963496  PMID: 40172095

ABSTRACT

Human papillomavirus (HPV) is associated with a significant global burden of precancerous lesions and cancer. People with HIV (PWH) are at higher risk of HPV infection and HPV‐related diseases. This systematic review was conducted to synthesize data on the burden of HPV infection and HPV‐related diseases among PWH. Studies published between January 2018–June 2023 were sourced from databases and conferences. Included were 221 publications containing epidemiological data on HPV infections and the clinical burden of HPV‐related diseases among PWH. The burden varied by geographical region, age, sex, and sexual orientation. Compared to people without HIV (PWoH), PWH had higher prevalence and incidence of HPV infection and HPV‐related diseases. Among PWH, the prevalence of anal HPV infection ranged between 44% and 83%; men had a higher prevalence and incidence of anogenital warts than women. The incidence of anal HPV infection was over two‐fold greater among transgender women with HIV and men who have sex with men with HIV than among their respective counterparts without HIV. Incident HPV‐related anal cancer was up to two‐fold higher among PWH than PWoH, and incident cervical cancer was up to six times higher among women with HIV than those without. The most prevalent high‐risk (hr) HPV genotypes with HPV‐related disease were vaccine genotype HPV16/18/52/58. HPV35 was one of the most prevalent genotypes with anal or cervical HPV infection among PWH of African descent. PWH also have a higher burden of concurrent HPV infections and HPV‐related diseases. This study calls for strengthening appropriate HPV vaccine delivery and increasing vaccine uptake among this high‐risk group, potentially by integrating HPV vaccination with routine HIV care.

Keywords: cervical cancer, HIV, HPV, HPV‐related cancer, human papillomavirus, PWH

1. Introduction

Human papillomavirus (HPV) is the most common sexually transmitted infection, and is associated with a significant burden of precancerous lesions and cancers globally [1, 2]. A prominent example is cervical cancer, the fourth most frequently diagnosed and the fourth leading cause of cancer death among women worldwide. Over 90% of global cervical cancer cases are caused by HPV.

There are > 200 HPV genotypes; however, about 15 of them are classified as high‐risk (hr) genotypes, and responsible for HPV‐related cancers [3, 4, 5]. Particularly, persistent HPV infections cause almost all cervical cancers as well as contribute to a substantial burden of anogenital and oropharyngeal cancers [6]. Moreover, HPV‐related cancers contribute to high morbidity and mortality rates and decreased quality of life of patients [7, 8]. HPV‐related diseases are also associated with high healthcare resource utilization and costs [7]. One study estimated that lifetime medical treatment costs in the United States (US) alone amount to $744 million [7, 8].

While HPV affects the general population, it poses unique challenges for people with human immunodeficiency virus (PWH) due to immune system dysfunction [1]. Globally, PWH were estimated over 39 million at the end of 2022 [9]. Although it is recognized that HPV infection and HPV‐related diseases among PWH represent a substantial healthcare burden globally, the evidence base communicating this burden is limited.

Understanding the burden of HPV in PWH is crucial for the implementation of effective prevention strategies, including HPV vaccination and optimizing clinical management including improvements of screening. This systematic review provides an understanding of the burden of HPV infections and HPV‐related diseases among PWH and identified remaining research gaps.

2. Methods

This is a systematic literature review that was performed following the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses (PRISMA) guidelines [10].

2.1. Search Strategy and Inclusion Criteria

A comprehensive search was conducted within the Ovid platform and included EMBASE, Medline, and Evidence‐Based Medicine Reviews (including Cochrane databases). Search strategies and supplementary searches of relevant conference proceedings with the full list of the conferences were included in Supplementary Table 1 (Supporting Information S1: Table S1). Publications reporting on epidemiological, clinical, humanistic, and economic outcomes among adults ( ≥ 18 years) with HIV with HPV infections or HPV‐related diseases were included. Randomized controlled trials, case studies or case reports, and review articles were excluded. Full eligibility criteria are in Supporting Information S1: Table S2.

The search was limited to publications from January 1, 2012, to June 5, 2023. Given the wealth of evidence identified following full‐text review, the time horizon for eligibility was shortened to publications from 2018 to 2023 for most recent and relevant outcomes, by excluding publications before 2018 from the analysis. Search strategies are presented in Supporting Information S1: Tables S3–S5. The main study outcomes of interest included the prevalence and incidence of HPV infection and HPV‐related diseases at different anatomical sites such as cervical, anogenital, oral, and other anatomical sites. In addition, the review captured study characteristics including age, gender, sexual orientation, and region.

2.2. Data Collection Procedure

Abstract and full‐text screening were conducted by two independent reviewers, with any differences resolved by a third reviewer. Data extraction was conducted by one reviewer and verified by a second reviewer, using a standardized data extraction form designed to capture study characteristics, methods, study population, subgroup characteristics, and reported outcomes. Assessment of study quality was conducted using Joanna Briggs Institute (JBI) Critical Appraisal Tools [11]. Assessment scales used according to study type are in Supporting Information S1: Figures S1–S3 and critical assessment is in Supporting Information S1: Figure S4.

2.3. Data Synthesis

Data captured from studies were synthesized narratively. The primary outcomes summarized and reported includes prevalence and incidence of HPV infections at different anatomical sites, and HPV‐related disease outcomes including cervical, anogenital, oral, and other anatomical sites related diseases. The synthesized prevalence and incidence of HPV infection and HPV‐related outcomes were presented by figures for visualization of data. Values from studies reporting on the same outcome type were used to calculate means or ranges provided within this review. When a study had anomalous values in comparison to the rest of the data set, the weighted mean was calculated based on study sample sizes to mitigate the effect of the anomalous value on the final mean.

3. Results

3.1. Study Selection and Population Characteristics

A total of 221 publications were included (Figure 1), reporting on data collected in Africa (n = 65), Europe (n = 49), the US and Canada (n = 40), Asia (n = 33), Central and South America (n = 23) and the Middle East (n = 1). Although this review primarily focused on studies that reported HPV burden in PWH, a subset of comparative studies (n = 109) that compared PWH versus PWoH were also included in this report.

Figure 1.

Figure 1

Open in a new tab

PRISMA flow diagram of included publications retrieved from databases and conferences.

Several studies have also reported on subgroups, such as women with HIV (WWH), and men who have sex with men (MSM). Full details of included publications can be found within the supplementary materials.

3.2. Epidemiology of HPV Infections

Overall, 184 publications included prevalence data on HPV infections, of which, six included multinational data. Cervical (n = 100 publications), anal (n = 93), and oral (n = 38) anatomical sites were the most reported on (Supporting Information S1: Figure S5). Publications reporting on the epidemiology of HPV infection at anogenital sites beyond anal and cervical (including penile, vulval and vaginal) were captured and included in this review, however not reported on separately here due to heterogenous and insufficient data, limiting the synthesis of these results. There was a lack of recent incidence data, with only 20 publications reporting on data ranging between 1996 and 2019.

Generally, the prevalence and incidence of anal, cervical, and oral HPV infections are consistently higher in PWH than PWoH (Figure 2A). In addition, hrHPV types and concurrent infection with multiple HPV genotypes were more common in PWH than PWoH (supplementary tables).

Figure 2.

Figure 2

Open in a new tab

(A) Summary of HPV prevalence across anal, cervical and oral sites by HIV status. Includes comparative publications only [12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34]. Publications reporting on multiple subpopulations have been included as separate data points. (B) Average prevalence of cervical HPV infection from publications reporting comparative data [12, 13, 14, 25, 26, 27, 28, 29, 30, 31]. (C) Average weighted prevalence of cervical HPV infection among WWH, stratified by geographic region [12, 13, 14, 25, 26, 27, 28, 29, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55]. Weighted prevalence was calculated according to the total sample size of the population from each region. (D) Average prevalence of anal HPV infection, stratified by patient population and HIV status; reporting only from publications with comparative data [20, 21, 22, 56]. (E) Average prevalence of anal HPV infection stratified by subpopulation [15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 52, 54, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78]. (F) Summary of any oral HPV infection, stratified by patient population and HIV status [16, 17, 19, 31, 32, 33, 34, 79]. HIV, human immunodeficiency virus; HPV, human papillomavirus; MWH, men with HIV; MSM, Men who have sex with men; MSMWH, men who have sex with men with HIV; MSW, Men who have sex with women; MSWWH, men who have sex with women with HIV; N, number; PWH, people with HIV; PWoH, people without HIV; WWH, women with HIV.

3.3. Cervical HPV Infections

Overall, 89 publications investigated cervical HPV prevalence, of which 10 included comparative data (Supporting Information S1: Tables S6 and S7). The prevalence of cervical HPV infections is substantially higher in WWH (Figure 2B), ranging between 20% and 98%, and with reports of up to six times higher prevalence than in women without HIV [12, 13]. The wide range is potentially due to geographical differences and age. HPV infection was on average approximately two times more prevalent in African than North American WWH (Figure 2C). The lowest prevalence of 20.2% was from the US, based on medical records data from 68,096 women aged 30–64 years, of which 608 were WWH [14]. This prevalence was significantly higher (p < 0.001) than that in women without HIV (6.5%) [14]. The highest prevalence of infection with one or more HPV type was 98.4%, reported from Kenya among 245 pregnant WWH aged 17–42 years and 85.5% carried at least one hrHPV type [35].

The reported prevalence and incidence of cervical HPV infection also varied with age across studies. Two publications reported that African women aged 25–39 years have a higher prevalence of cervical HPV infection compared to older women [80, 81], and another from Morocco found the highest prevalence in women aged 30–40 years [82]. Teixeira et al. (2018) reported that the prevalence of hrHPV was higher in Brazilian women (N = 299) aged ≥ 36 years and peaked in women ≥ 50 years [83]. While there were limited age‐stratified incidence data on cervical HPV infection (Supporting Information S1: Table S8), a study from Tanzania reported that incidence of cervical hrHPV infection was higher among WWH aged 25–29 years and lowest in 50–60 years old; both WWH and women without HIV had decreasing HPV incidence rates with increasing age [84]. While incidence was higher among WWH than women without HIV in all age groups, the smallest difference in incidence rate was seen among women aged 25–29 years and the largest difference in the incidence rate was among women 50–60 years [84].

3.4. Anal HPV Infection

Studies comparing the prevalence and incidence of anal HPV infection in PWH and PWoH were sparse, except in the MSM population (Supporting Information S1: Tables S9–S12). The available data shows that the prevalence of anal HPV infection among PWH varied across subpopulations. Anal HPV prevalence was three times higher in WWH than in women without HIV, and over two‐fold higher in men with HIV (MWH) than men without HIV. MSM with HIV had a prevalence of anal HPV infection 1.4 times higher than MSM without HIV (Figure 2D). MSM with HIV had the highest prevalence whereas men with HIV who have sex with women the lowest (Figure 2E). Therefore, publications that report anal HPV infection data in PWH varied by the proportion of these subgroups included in the studies.

Regional analysis revealed that although MSM with HIV have comparable high prevalences across all geographical regions, those in Europe have the highest prevalence of any anal HPV infection with prevalence rates up to 91% [15, 16, 17, 18, 19, 57, 58, 59, 60, 61, 62, 63, 64], compared with Central and South America (86.1%) [85], North America (83.5%) [65, 86], Africa (83.3%) [20, 21, 22, 87], Asia (77.8%) [23, 66, 67, 68], and Oceania (74.0%) [69].

As with anal HPV infection prevalence, the incidence is high among MSM with HIV (Supporting Information S1: Table S13) [69, 88, 89]. One US study found the incidence rate of anal infections with hrHPV genotypes covered by the nonavalent vaccine (HPV16/18/31/33/45/52/58) in MSM with HIV was about two times higher than in MSW with HIV (15.6 vs. 7.6 per 100 person‐years) [90]. Furthermore, the incidence of anal HPV infection was over two‐fold greater in men and transgender women with HIV than their counterparts without HIV [91, 92].

The association of age with anal HPV infection varied by region and sexual orientation. One study found anal HPV infection peaked at ages 25–29 years in Italian MSM with HIV. Another study noted there was no significant difference in anal hrHPV infection between French MSM with HIV aged 35–45 and ≥ 55 years. PWH from Colombia with a history of anal intercourse aged > 50 years had lower risk for hrHPV infection than those aged < 30 years [61, 93, 94].

3.5. Oral HPV Infection

Few publications reported oral HPV infection prevalence in PWH compared to those without HIV (Supporting Information S1: Table S14 and S15). Oral HPV infection was 1.5–3 times more prevalent in PWH than PWoH (Figure 2F). Most publications reported a lower overall prevalence of oral HPV infections among PWH compared to anal or cervical HPV infection prevalence, ranging from 5.6% to 15.0% (Figure 2A). However, two studies from Mexico reported higher prevalence of oral HPV infection of up to 92.5% of 174 Mexican WWH, and 55.7% of 97 Mexican PWH using a highly sensitive assay [95, 96].

Two studies found that incident oral HPV infections were higher among PWH than PWoH, particularly in MSM [96, 97], however additional studies are needed to draw meaningful conclusions (Supporting Information S1: Table S16).

3.6. High‐Risk HPV Genotype Distribution

3.6.1. Cervical hrHPV Infections in WWH

Variability exists across studies on the number of HPV genotypes tested and in general, data indicated notable differences in genotype distribution across regions. In Africa, HPV52 was the most prevalent, followed by 35 and 51, while HPV16 in Asia and HPV31 in Europe were the most prevalent genotypes (Figure 3).

Figure 3.

Figure 3

Open in a new tab

Average cervical hrHPV genotype distribution among WWH across regions. 9v, nonavalent; HPV, human papillomavirus; hrHPV, high‐risk human papillomavirus; N, number of publications; WWH, women with HIV.

3.6.2. Anal hrHPV Infections in PWH

HPV16 is, on average, the most prevalent genotype globally. While there are differences in geographical distribution, the most notable was the higher prevalence of HPV35 among African PWH, similar to that of HPV16 (Figure 4).

Figure 4.

Figure 4

Open in a new tab

Average anal hrHPV genotype distribution among PWH across regions. 9v, nonavalent; HPV, human papillomavirus; hrHPV, high‐risk human papillomavirus; N, number of publications; PWH, people with HIV.

3.6.3. Oral hrHPV Infections in PWH

Although studies on oral HPV infection is limited, available evidence suggested that in Europe HPV56 and HPV66 and in North America HPV18, HPV16, and HPV39 were the most prevalent oral hrHPV types (Figure 5).

Figure 5.

Figure 5

Open in a new tab

Average oral hrHPV genotype distribution among PWH across regions. 9v, nonavalent; HPV, human papillomavirus; hrHPV, high‐risk human papillomavirus; N, number of publications; PWH, people with HIV.

3.7. HPV Concurrent Infection With Multiple Genotypes

Multiple studies conducted across Europe [15, 16, 18], Africa [20, 21, 87, 98], and Asia [23, 24] suggest that MSM with HIV have a higher prevalence of anal HPV concurrent infection with multiple genotypes compared to MSM without HIV (Supporting Information S1: Table S17). Similar results were reported for cervical infections. One African based study that included four countries found that concurrent infection with multiple hrHPV genotypes were significantly more prevalent among WWH than women without HIV (43.0% vs. 21.6%, respectively; p = 0.01) [80]. While comparative data for oral HPV infection with multiple genotypes was limited, a recent US study reported that 9.0% of 245 PWH and 1.0% of 198 PWoH had oral infection with multiple genotypes [32].

3.8. Risk Factors

Although not the primary focus of this review, several publications cited low CD4 counts ( < 200 cells/μl) [39, 77, 99, 100], detectable HIV viral load ( > 50 copies/mL) [31, 44, 50, 59, 74, 95, 101, 102], and a shorter duration on antiretroviral therapy (ART) [59, 73, 89, 99, 103, 104] as risk factors for HPV infection and HPV‐related diseases in PWH and, therefore, contribute to increased disease burden of HPV in PWH. However, another study showed that even women receiving effective ART and with high CD4 counts are at increased risk of HPV infection and have higher prevalence of hrHPV infections [51]. Other reported risk factors for HPV infection and related diseases include high‐risk sexual behaviors such as sexual debut < 15 years [92, 100, 101, 105, 106, 107, 108], and having > 5 lifetime sexual partners [32, 52, 95, 100, 101, 104, 108, 109, 110, 111].

3.9. Burden of HPV‐Related Diseases

Several studies (n = 83) reported on the burden of HPV‐related diseases, including precancers, invasive cancers and anogenital warts (AGW), among which cervical abnormalities (n = 48) and cancers (n = 17) were the most reported, followed by anal abnormalities (n = 10) and cancers (n = 8). Supporting Information S1: Figure S6 shows a breakdown of disease burden by anatomical site. The burden of HPV‐related disease at anogenital sites beyond anal and cervical (including penile, vulval and vaginal) were captured in this review, however, were not reported on separately here due to heterogenous and insufficient data, limiting the synthesis of these results. Generally, the prevalence, incidence and risk of anal, cervical, and oral HPV‐related diseases was higher among PWH than PWoH.

3.10. HPV‐Related Cervical Precancers

Cervical precancer lesions was more prevalent in WWH than women without HIV, with the global prevalence of any cervical abnormality being, on average, 1.5–3 times higher in WWH (Supporting Information S1: Table S18 and S19). This prevalence ranged between 5.4% and 31.0% for WWH and 1.8%–20.4% for women without HIV, with higher prevalence reported in Central and South America than North America and Asia (Figure 6). Similar results were seen for high‐grade abnormalities only (Figure 7).

Figure 6.

Figure 6

Open in a new tab

Average weighted prevalence of any cervical abnormality in women with HIV and women without HIV by region [12, 14, 31, 105, 110, 112, 113]. Europe not included due to lack of data. Any cervical abnormality across publications was defined by the inclusion of atypical squamous cells of undetermined significance (ASC‐US), low‐grade squamous intraepithelial lesions (LSIL), high‐grade squamous intraepithelial lesions (HSIL), atypical granular cells of undetermined significance (AG‐US), atypical squamous cells not excluding high grade (ASC‐H), except for one Asian study which did not specify what this encompassed [113]. Abbreviations: HIV: human immunodeficiency virus.

Figure 7.

Figure 7

Open in a new tab

(A) Prevalence of high‐grade cervical abnormalities (HSIL, ASC‐H, CIN2 + ) among women with HIV; North America: US [112, 114]; Central and South America: Colombia [105], Brazil [31, 83, 115]; Europe: Italy [49, 116], Belgium [117], Spain [118]; Africa: South Africa [119], Tanzania [27, 108], Burundi [120], Nigeria [28, 121, 122], Asia: India [13, 46, 104, 123, 124], China [101, 125]; B: Prevalence of high‐grade cervical abnormalities (HSIL, ASC‐H, CIN2 + ) in women without HIV only; North America: US [112], Central and South America: Colombia [105], Brazil [31]; Africa: South Africa [119], Kenya [126], Tanzania [27, 108], Burundi [120], Nigeria [28, 121, 122]; Asia: India [13]. French data from Bouassa et al. (2019) not included due to study population being African migrants [127]. ASC‐H, atypical squamous cells not excluding high grade; CIN, cervical intraepithelial neoplasia; HSIL, high‐grade squamous intraepithelial lesions; NR, not reported.

While age‐stratified data were scarce, of the 34 publications reporting prevalence of cervical precancer abnormalities, most cases were among WWH within the 30–45‐year age range, suggesting that cervical abnormalities may be more prevalent in younger age groups.

3.11. HPV‐Related Cervical Cancer

Incident cervical cancer was 1.5–6.6 times greater among WWH in comparison to their counterparts without HIV, dependent on the histological subtype of cancer investigated (Supporting Information S1: Tables S20 and S21) [128, 129].

The highest prevalence of cervical cancer were reported in those with the mean ages between 30 and 55 years [13, 27, 130]. While age‐stratified cervical cancer prevalence and incidence data in WWH were limited, three studies reported higher incidence and prevalence rates between 35 and 54 years of age than those < 35 years or > 54 years. Comparative data suggests that cervical cancer prevalence peaks among younger WWH (35–44 years) in comparison to women without HIV (peak at ≥ 55 years) [129].

3.12. HPV‐Related Anal Abnormalities

Comparative studies (n = 4) reported prevalence of HPV‐related anal abnormalities 1.7–2.1 times higher among PWH compared to PWoH, with variation due to the study subpopulation and type of anal abnormality investigated (Supporting Information S1: Figure S7 and Table S22). Sex differences influence the burden of anal abnormalities. MWH had higher prevalence and incidence of anal abnormalities than WWH in North America and Asia, although additional data may be required to confirm this finding [110, 131, 132]. People with HPV‐mediated anal lesions had faster rates of progression to carcinoma in situ (CIS) and to invasive carcinoma in people with versus without HIV, which was further enhanced by low CD4 counts [133].

3.13. HPV‐Related Anal Cancer

Two publications reported a higher incidence and risk of anal cancer among PWH than PWoH (Table S23). A study in the US showed age‐adjusted incidence rate of anal cancer among American women with HIV and without HIV was 12.6 (95% CI: 0–30.9) and 8.4 (95% CI: 0.8–15.9) per 100,000 person‐years, respectively [128]. Similarly, PWH were at higher risk of HPV‐related anal disease progression than PWoH (high‐grade squamous intraepithelial lesions [HSIL] to CIS or further; HR: 1.43; p = 0.02) and CIS to squamous cell carcinoma [SCC; HR: 2.08; p = 0.03]) [134]. Additional studies from the US (n = 3) reported that MWH had a higher prevalence and incidence of HPV‐related anal cancer than WWH [131, 135, 136]. There were no data reporting on the incidence of anal cancer among MSM with HIV.

3.14. HPV‐Related Oral and Head and Neck Cancer

There were limited comparative data reporting on oral and head and neck cancers (Table S24). A French study reported that incident head and neck cancer was 2.6 times higher among PWH than PWoH (79.1 vs. 30.7 per 100,000 person‐years), and noted an association with age [137]. PWH aged 50–59 years had the highest incidence rate (122.6 per 100,000 person‐years) compared to those aged 18–39 years, 40–49 years, and ≥ 60 years (0, 66.3, and 110.9 per 100,000 person‐years, respectively) [137].

The epidemiology of oral cancer differed with ethnicity; in the US, non‐Hispanic black individuals had a higher burden of oral cancer than Hispanic and non‐Hispanic white individuals [135, 136].

3.15. Genotype Distribution in HPV‐Related Diseases

HPV genotype distribution data among PWH with HPV‐related disease was identified as an important research gap within the current literature. One study highlighted that, in anal condyloma tissues, HPV16, HPV52 and HPV58 high‐risk genotypes occurred in higher frequencies among MSM with HIV versus without HIV [138].

Similar to HPV infections, available data indicated that PWH with HPV‐related diseases had an overall higher number of HPV genotypes [105]. American PWH with HPV‐mediated anal lesions, including anal intraepithelial neoplasia (AIN) 1, 2, 3, low‐grade squamous intraepithelial lesions (LSIL), HSIL or invasive SCC, had a higher overall genotype diversity than PWoH (7 vs. 4 median number of genotypes, respectively) [133]. This higher HPV strain diversity was associated with faster progression from AIN1/LSIL to AIN2‐3/HSIL [133]. Additionally, PWH with HPV‐mediated anal lesions had significantly higher infection rates with HPV strains 35, 39, 52, 53, 56, 58, 59, 66, and 68. HPV39, 58, 66, and 67 were associated with faster progression in both PWH and PWoH.

Kremer et al. (2018) noted that among 123 and 22 South African WWH with cervical intraepithelial neoplasia (CIN) 3 and invasive cervical cancer (ICC), respectively, HPV16 was the most prevalent genotype (CIN3: 31.7%; ICC: 45.5%), followed by HPV18 (CIN3: 13.6%; ICC: 13.6%), and HPV45, (CIN3: 13.6%; ICC: 13.6%) [139]. Tawe et al. (2020) also reported similar findings with the most prevalent genotype being HPV16 (47.7%) among 88 Botswanan WWH with ICC [140]. Teixeira et al. (2018) reported that among 21 and 10 Brazilian WWH with cervical LSIL and HSIL, respectively, 52.3% and 60.0% were infected with genotypes HPV56/59/66, respectively, while 23.8% and 50.0% were infected with HPV16, respectively [83]. A study from China reported that hrHPV infections increased with increasing severity of histological abnormalities from 17.6% in women with normal findings to 88.9% in those with LSIL and 92.0% for HSIL. HPV16, HPV52, and HPV58 were the most common hrHPV types in women with HSIL [101]. Another study from Belgium reported that the most common hrHPV types in abnormal cytology were HPV31, HPV52, and HPV66 [117].

4. Discussion

This study showed that PWH have a higher prevalence and incidence of HPV infection than PWoH across all anatomical sites. Prevalent cervical infections were up to six times higher among WWH than women without HIV depending on the region, while prevalent anal and oral HPV infections were about twice as high among PWH than PWoH. These results are consistent with previous systematic reviews and studies conducted across broader and earlier time periods. Previous systematic review that synthesized studies published between 1986 and 2017 reported that the prevalence of anal HPV infection was 1.3–1.4 times higher among PWH, while another systematic review conducted in 2015 reported that oral HPV infection prevalence 1.5 times higher among HIV‐positive MSM compared to HIV‐negative MSM [141, 142]. However, contrary to the findings of this review, a relatively older study conducted in 2008 reported comparable prevalences of cervical HPV infection between South African WWH and women without HIV [143].

Moreover, HPV‐related diseases were consistently higher among PWH than PWoH. Compared to women without HIV, cervical precancers were 1.5–3.0 times more prevalent in WWH, and incident cervical cancers were up to six times higher in WWH, perhaps suggesting a faster progression of precancer to invasive cervical cancer in PWH. Furthermore, the prevalence of anal abnormalities was about two‐fold higher among PWH than PWoH, and the incidence of head and neck cancer was also over two times higher among PWH than PWoH.

The prevalences and incidences of HPV infection and related diseases varied depending on subpopulations and anatomical sites. MSM with HIV had a higher prevalence of anal HPV infection compared to WWH or MWH who have sex with women. Average prevalence differences between MSM with and without HIV were smaller than differences in other subgroups (e.g., WWH vs. women without HIV), suggesting that sexual behavior has a greater influence on the prevalence of anal HPV infection than HIV status in this subpopulation. This aligns with findings from a recent meta‐analysis, which reported that the most important population‐level determinant of anal HPV infection, aside from HIV status, was sexual orientation [144].

As with HPV infections, the burden of HPV‐related anal diseases, including invasive cancer and both high‐ and low‐grade anal abnormalities, is higher among men with HIV than women with HIV, 2‐to‐7 fold higher anal precancers and 2‐to‐25 fold higher anal cancer, potentially due to the presence of MSM within male study populations [141]. The risk of progression from precancer to anal carcinoma in situ and to invasive anal carcinoma was reported to be about two‐fold higher in PWH versus PWoH. Receptive anal sex is a well‐documented risk factor for anal HPV infection in the literature and absence of formal guidelines recommending anogenital screening for men across most countries exacerbates the issue, leading to recurrent anal HPV infections and the development of HPV‐related anal diseases [135, 145].

The burden of HPV infection and HPV‐related disease among PWH varied by geographical region, however comparative studies are limited. For example, a higher prevalence of cervical HPV infection and high‐grade cervical abnormalities has been observed in Africa versus North America and Europe. Geographical differences in cervical HPV infection and related disease may be attributed to variations in availability of HPV vaccination, low HPV vaccine uptake, lack of cervical screening, and decreased access to healthcare facilities, leading to high rates of persistent HPV infections in certain countries [146]. Additional research into HPV infection and related diseases in PWH across geographical regions is required to categorize the burden.

The burden of HPV infection and HPV‐related disease also varies with age. Some studies reported a higher prevalence of cervical HPV infection among women aged 25–39 years than older women, while others found prevalent cervical infection with hrHPV increased among women aged ≥ 36 years and peaked in women aged ≥ 50 years. The reasons for variations with age are unclear due to limited data and heterogeneity of populations within the studies; however, it was suggested that the prevalence of hrHPV peaking among ≥ 50 years was attributed to higher rates of HPV persistence due to impaired clearance and reactivation of latent infection during the perimenopausal period rather than new HPV infection acquisition [83, 147]. Additionally, changes in sexual behavior during middle age may also play a role in prevalence increases among older women [83]. These findings suggests the importance of expanding vaccination to the older ages, beyond the current recommendations.

Alarmingly, incident cervical cancer rates are highest among younger WWH, specifically those aged 35–54 years, compared to those aged > 55 years. Comparative data also suggested that cervical cancer prevalence peaked among younger WWH (35–44 years) in contrast to women without HIV, for whom prevalence peaks at age ≥ 55 years. Similarly, high prevalence of precancer cervical lesions in WWH was among those aged within the 30–45‐years range, suggesting that cervical precancers and cancer may be more prevalent at younger age in WWH than in women without HIV, and perhaps indicating faster progression to cancer in WWH. A previous systematic review noted that incident cervical cancer was highest among women without HIV of age > 70 years in most geographical regions [148].

Analysis of hrHPV genotypes among PWH revealed a variable distribution across most geographical regions. In cervical HPV infections, HPV16 and HPV31 are the most prevalent in Asia, while HPV52 and HPV35 are the most prevalent in Africa. This is consistent with two published systematic reviews that identified HPV35 one of the most prevalent genotypes in cervical HPV infections among African women [149, 150]. Among PWH with anal HPV infection, HPV16 was the most prevalent genotype globally, whereas HPV35 had an elevated prevalence in Africa. Finally, there were no clear distribution trends among PWH with oral infection due to a paucity of data. Whilst our findings suggest genotype prevalence can vary, HPV35 remains a highly prevalent genotype in African populations, and it is not currently targeted by vaccination.

Genotype distribution data for PWH with HPV‐related disease were limited, indicating a significant gap in the evidence. It has been noted that high‐risk, vaccine‐preventable genotypes (HPV16, 18, and 45) and infection with multiple genotypes (HPV56/59/66) were the most prevalent among African and Mexican WWH with cervical disease [83, 117, 139]. Interestingly, among Asian MSM with anal condylomas, hrHPV genotypes were found at significantly higher frequencies in MSM with HIV than counterparts without HIV, despite the fact that anal condylomas are typically caused by low‐risk HPV types [138].

PWH with HPV‐related anal diseases were concurrently infected with a wider diversity of genotypes compared to PWoH. This is may be due to a multitude of reasons, such as immunosuppression resulting from low CD4 cell counts, increased high‐risk sexual behavior, or an immune response to anal lesions that may in turn mediate infection with rare HPV types [133]. Further research into the associated genotypes with HPV‐related diseases can provide key evidence to support vaccination programs aimed at alleviating the disease burden.

Several publications have reported that low CD4 counts, detectable HIV viral load, and a shorter duration on ART are risk factors for HPV infection and HPV‐related diseases in PWH. However, some research has also found that WWH who are receiving effective ART and have high CD4 counts still face an increased risk of HPV, indicating that other factors are at play in addition to immune depression [51].

The findings of this review indicate substantial heterogeneity in reporting across anatomical sites and patient subpopulations. Therefore, careful interpretation of results is required. Notably, heterogeneity in the reporting of stratified results, particularly among subpopulations such as MSM and MSW, has limited our conclusions on the impact that HIV may have on these groups. Heterogeneity may stem from differences in data collection methods‐ many publications captured genotype distribution data pertaining only to genotypes in the 9‐valent vaccine or fewer‐ as well as diversity in methodology (e.g., diagnosis via cytological/histological tests or visual inspections), sociodemographic characteristics and risk exposures within study populations. Furthermore, there is a lack of consensus on the definitions within the literature, including on the risk status and oncogenicity of various HPV genotypes. This has resulted to variations in prevalence and incidence figures across publications, with the same genotype being classified as high risk in one study and low risk in another. Publications investigating HPV‐related diseases often lacks standardized criteria for defining anogenital abnormalities, such as atypical squamous cells of undetermined significance. Moreover, some studies did not specify whether oral disease burden was HPV‐related, resulting in limited data for this anatomical site. Geographical differences should be interpreted with caution, as they may include populations who have recently migrated, affecting the burden of HPV infection and disease across countries [127].

5. Conclusion

This systematic review confirms that PWH have a significantly higher burden of HPV infections as well as HPV‐related precancers and invasive cancers than PWoH. The burden varies with age, gender, sexual orientation, and geographic region. Comparisons with studies from earlier time periods suggest that the disparity in the burden of cervical HPV infection rates has increased in recent years among WWH in comparison to women without HIV. This trend may be attributed to the success of HPV vaccination programs that have primarily focused on vaccinating younger women, with less emphasis on increasing vaccination access in those living with HIV. To address this disparity, HPV prevention strategies, such as vaccination should be bolstered among PWH, especially in regions with high HIV prevalence. Populations that warrant targeted HPV prevention strategies with vaccination include WWH due to their increased cervical hrHPV infection prevalence and cervical cancer incidence, as well as MSM with HIV due to an elevated risk of anal HPV infection, compared to other subgroups [147]. Among WWH with cervical HPV infections, vaccine preventable genotypes were found to be the most prevalent. The prevalence of these genotypes suggests that the current vaccination and screening strategy may be insufficient for WWH. Future prevention measures should also target prevalent oncogenic genotypes that are not currently covered by vaccines, such as HPV35, which has been frequently reported among PWH in Africa. Furthermore, the high prevalence of concurrent infection with multiple HPV genotypes underscores the need to roll out a higher valent HPV vaccine to gain maximum protection. Lastly, implementation of HPV vaccination by integrating it into routine HIV care and clinics providing HIV prevention for high‐risk groups may provide a valuable opportunity to increase HPV vaccine uptake while also promoting efficiency in delivery.

Author Contributions

Alisa Chowdhary, Jia Pan, and Ana Costa developed the study protocol, performed the literature search, drafted the study results, developed the first draft of the manuscript, and critically reviewed the manuscript drafts. Xuedan You and Ya‐Ting Chen were involved in the conception of the study, and review of the protocol development. Bekana K. Tadese, Tidiane Ndao, Xuedan You, Ya‐Ting Chen, and Joseph E. Tota were involved in the review of the study results, interpretations, and critical review of versions of the manuscript drafts. Nelly Mugo was involved in the review of the study results and critical review of the manuscript drafts. All authors reviewed the results from the systematic literature review, reviewed manuscript drafts, and approved the final version for submission.

Conflicts of Interest

B.K.T., X.Y., T.N., J.E.T., and Y.C. are employees of Merck & Co. Inc. Rahway, NJ, USA. Alisa Chowdhary, Jia Pan, and Ana Costa are employees of Adelphi Values PROVE and were funded by Merck Sharp & Dohme LLC, a subsidiary of Merck & Co. Inc. Rahway, NJ, USA to conduct this research. Nelly Mugo is employee of Kenya Medical Research Institute, Nairobi City, Kenya.

Supporting information

Supporting information.

JMV-97-e70274-s001.docx (1.4MB, docx)

Acknowledgments

The authors would like to thank the Adelphi Values PROVE team who contributed to the literature search and data extraction. This study was funded by Merck Sharp & Dohme LLC, a subsidiary of Merck & Co. Inc. Rahway, NJ, USA.

Data Availability Statement

Data for this manuscript was from published studies, all of which have been cited appropriately in text and tables.

References

  • 1. Kombe Kombe A. J., Li B., Zahid A., et al., “Epidemiology and Burden of Human Papillomavirus and Related Diseases, Molecular Pathogenesis, and Vaccine Evaluation,” Frontiers in Public Health 8 (2020): 552028, 10.3389/fpubh.2020.552028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2. de Martel C., Plummer M., Vignat J., and Franceschi S., “Worldwide Burden of Cancer Attributable to HPV by Site, Country and HPV Type,” International Journal of Cancer 141, no. 4 (2017): 664–670, 10.1002/ijc.30716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Muñoz N., Bosch F. X., de Sanjosé S., et al., “Epidemiologic Classification of Human Papillomavirus Types Associated With Cervical Cancer,” New England Journal of Medicine 348, no. 6 (2003): 518–527, 10.1056/NEJMoa021641. [DOI] [PubMed] [Google Scholar]
  • 4. Choi Y. J. and Park J. S., “Clinical Significance of Human Papillomavirus Genotyping,” Journal of Gynecologic Oncology 27, no. 2 (2016): e21, 10.3802/jgo.2016.27.e21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Chen Z., Schiffman M., Herrero R., et al., “Classification and Evolution of Human Papillomavirus Genome Variants: Alpha‐5 (HPV26, 51, 69, 82), Alpha‐6 (HPV30, 53, 56, 66), Alpha‐11 (HPV34, 73), Alpha‐13 (HPV54) and Alpha‐3 (HPV61),” Virology 516 (2018): 86–101, 10.1016/j.virol.2018.01.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6. Malagón T., Franco E. L., Tejada R., and Vaccarella S., “Epidemiology of HPV‐Associated Cancers Past, Present and Future: Towards Prevention and Elimination,” Nature Reviews Clinical Oncology 21, no. 7 (2024): 522–538, 10.1038/s41571-024-00904-z. [DOI] [PubMed] [Google Scholar]
  • 7. Ong K. J., Checchi M., Burns L., Pavitt C., Postma M. J., and Jit M., “Systematic Review and Evidence Synthesis of Non‐Cervical Human Papillomavirus‐Related Disease Health System Costs and Quality of Life Estimates,” Sexually Transmitted Infections 95, no. 1 (2019): 28–35, 10.1136/sextrans-2018-053606. [DOI] [PubMed] [Google Scholar]
  • 8. Chesson H. W., Laprise J.‐F., Brisson M., Martin D., Ekwueme D. U., and Markowitz L. E., “The Estimated Lifetime Medical Cost of Diseases Attributable to Human Papillomavirus Infections Acquired in 2018,” Sexually Transmitted Diseases 48, no. 4 (2021): 278–284, 10.1097/olq.0000000000001379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. World Health Organization . HIV and AIDS, https://www.who.int/news‐room/fact‐sheets/detail/hiv‐aids.
  • 10. Page M. J., McKenzie J. E., Bossuyt P. M., et al., “The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews,” BMJ 372 (2021): n71, 10.1136/bmj.n71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. Higgins J., Thomas J., Chandler J., et al., Cochrane Handbook for Systematic Reviews of Interventions Version 63 (2022). [Google Scholar]
  • 12. James Kinotia N., Muturib M., Kamauc L., and Lwembed R., “Human Papillomavirus Types Prevalence and Their Association With Cervical Dysplasia Among HIV and Non‐HIV Infected Women Attending Reproductive Health Clinics in Eastern Kenya,” African Health Sciences 22, no. 1 (2022): 106–114, 10.4314/ahs.v22i1.14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13. Jain B. B., Adhikary T., Sadhukhan P. C., and Nandi A., “Human Papilloma Virus Infection of Uterine Cervix and Spectrum of Cervical Pathology in Human Immunodeficiency Virus/AIDS,” Journal of Cancer Research and Therapeutics 17, no. 6 (2021): 1462–1467, 10.4103/jcrt.JCRT_552_19. [DOI] [PubMed] [Google Scholar]
  • 14. Castle P. E., Befano B., Schiffman M., et al., “A Comparison of High‐Grade Cervical Abnormality Risks in Women Living With and Without Human Immunodeficiency Virus Undergoing Routine Cervical‐Cancer Screening,” Preventive Medicine 162 (2022): 107157, 10.1016/j.ypmed.2022.107157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15. Donà M. G., Benevolo M., Latini A., et al., “Anal Cytological Lesions and HPV Infection in Individuals at Increased Risk for Anal Cancer,” Cancer Cytopathology 126, no. 7 (2018): 461–470, 10.1002/cncy.22003. [DOI] [PubMed] [Google Scholar]
  • 16. Nemcova J., Riegert J., Cerna K., et al., “Prevalence of Oral and Anal Human Papillomavirus Infection in Czech Predominantly Hiv‐Positive Men Having Sex With Men ‐ Data From a Previously Unreported Population,” International Journal of STD & AIDS 33, no. 12 (2022): 1054–1064, 10.1177/09564624221123869. [DOI] [PubMed] [Google Scholar]
  • 17. Rollo F., Latini A., Benevolo M., et al., “Concurrent and Concordant Anal and Oral Human Papillomavirus Infections Are not Associated With Sexual Behavior in At‐Risk Males,” Pathogens 10, no. 10 (2021): 1254, 10.3390/pathogens10101254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18. Szabó E., Kósa C., Babarczi E., et al., “Prevalence of Anal Human Papillomavirus Infection in Hungarian Men Who Have Sex With Men,” Pathology & Oncology Research 24, no. 3 (2018): 671–677, 10.1007/s12253-017-0292-5. [DOI] [PubMed] [Google Scholar]
  • 19. Ucciferri C., Tamburro M., Falasca K., Sammarco M. L., Ripabelli G., and Vecchiet J., “Prevalence of Anal, Oral, Penile and Urethral Human Papillomavirus in Hiv Infected and HIV Uninfected Men Who Have Sex With Men,” Journal of Medical Virology 90, no. 2 (2018): 358–366, 10.1002/jmv.24943. [DOI] [PubMed] [Google Scholar]
  • 20. Bouassa R. S. M., Simaleko M. M., Camengo S. P., et al., “Unusual and Unique Distribution of Anal High‐Risk Human Papillomavirus (HR‐HPV) Among Men Who Have Sex With Men Living in the Central African Republic,” PLoS One 13, no. 5 (2018): e0197845, 10.1371/journal.pone.0197845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21. Koyalta D., Mboumba Bouassa R. S., Maiga A. I., et al., “High Prevalence of Anal Oncogenic Human Papillomavirus Infection in Young Men Who Have Sex With Men Living in Bamako, Mali,” Infectious Agents and Cancer 16, no. 1 (2021): 51, 10.1186/s13027-021-00385-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22. Oo M. M., Moore S., Gibbons S., et al., “High Prevalence of Vaccine‐Preventable Anal Human Papillomavirus Infections Is Associated With HIV Infection Among Gay, Bisexual, and Men Who Have Sex With Men in Nairobi, Kenya,” Cancer Medicine 12, no. 12 (2023): 13745–13757, 10.1002/cam4.6008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23. Somia I. K. A., Teeratakulpisarn N., Jeo W. S., et al., “Prevalence of and Risk Factors for Anal High‐Risk HPV Among HIV‐Negative and HIV‐Positive Msm and Transgender Women in Three Countries at South‐East Asia,” Medicine (United States) 97, no. 10 (2018): e9898, 10.1097/MD.0000000000009898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24. Liu X., Lin H., Chen X., et al., “Prevalence and Genotypes of Anal Human Papillomavirus Infection Among HIV‐Positive vs. HIV‐Negative Men in Taizhou, China,” Epidemiology and Infection 147 (2019): e117, 10.1017/S0950268818003205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. Ermel A., Tonui P., Titus M., et al., “A Cross‐Sectional Analysis of Factors Associated With Detection of Oncogenic Human Papillomavirus in Human Immunodeficiency Virus‐Infected and Uninfected Kenyan Women,” BMC Infectious Diseases 19, no. 1 (2019): 352, 10.1186/s12879-019-3982-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. Lieber M., Reynolds C. W., Lieb W., McGill S., and Beddoe A. M., “Human Papillomavirus Knowledge, Attitudes, Practices, and Prevalence Among Men Who Have Sex With Men in Monrovia, Liberia,” Journal of Lower Genital Tract Disease 22, no. 4 (2018): 326–332, 10.1097/LGT.0000000000000436. [DOI] [PubMed] [Google Scholar]
  • 27. Mbuya W., McHaro R., Mhizde J., et al., “Depletion and Activation of Mucosal CD4 T Cells in HIV Infected Women With HPV Associated Lesions of the Cervix Uteri,” PLoS One 15, no. 10 October (2020): e0240154, 10.1371/journal.pone.0240154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28. Ogechukwu Okoye J., Ajuluchukwu Ngokere A., Erinle C., and Mbamalu C., “Co‐Existence of Herpes Simplex Virus Type 2 and Two Other Oncoviruses Is Associated With Cervical Lesions in Women Living With HIV in South‐Western Nigeria,” African Health Sciences 20, no. 3 (2020): 1015–1023, 10.4314/ahs.v20i3.4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29. Omire A., Budambula N. L. M., Kirumbi L., et al., “Cervical Dysplasia, Infection, and Phylogeny of Human Papillomavirus in HIV‐Infected and HIV‐Uninfected Women at a Reproductive Health Clinic in Nairobi, Kenya,” BioMed Research International 2020 (2020): 4945608, 10.1155/2020/4945608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30. Nijhawan P., Carraro A., Vita S., et al., “Systemic, Mucosal Immune Activation and Psycho‐Sexual Health in ART‐Suppressed Women Living With HIV: Evaluating Biomarkers and Environmental Stimuli,” Viruses 15, no. 4 (2023): 960, 10.3390/v15040960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31. Suehiro T. T., Damke G. M. Z. F., Damke E., et al., “Cervical and Oral Human Papillomavirus Infection in Women Living With Human Immunodeficiency Virus (HIV) and Matched HIV‐Negative Controls in Brazil,” Infectious Agents and Cancer 15, no. 1 (2020): 31, 10.1186/s13027-020-00301-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32. Riddell J., Brouwer A. F., Walline H. M., et al., “Oral Human Papillomavirus Prevalence, Persistence, and Risk‐Factors in HIV‐Positive and HIV‐Negative Adults,” Tumour Virus Research 13 (2022): 200237, 10.1016/j.tvr.2022.200237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Gheit T., Rollo F., Brancaccio R. N., et al., “Oral Infection by Mucosal and Cutaneous Human Papillomaviruses in the Men Who Have Sex with Men From the OHMAR Study,” Viruses 12, no. 8 (2020): v12080899, 10.3390/v12080899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34. Oliver S. E., Gorbach P. M., Gratzer B., et al., “Risk Factors for Oral Human Papillomavirus Infection Among Young Men Who Have Sex With Men ‐ 2 Cities, United States, 2012‐2014,” Sexually Transmitted Diseases 45, no. 10 (2018): 660–665, 10.1097/OLQ.0000000000000845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. Vyankandondera J., Wambua S., Irungu E., et al., “Type‐Specific Human Papillomavirus Prevalence, Incident Cases, Persistence, and Associated Pregnancy Outcomes Among HIV‐Infected Women in Kenya,” Sexually Transmitted Diseases 46, no. 8 (2019): 532–539, 10.1097/OLQ.0000000000001029. [DOI] [PubMed] [Google Scholar]
  • 36. Guthrie B. L., Rositch A. F., Cooper J. A., et al., “Human Papillomavirus and Abnormal Cervical Lesions Among HIV‐Infected Women in Hiv‐Discordant Couples From Kenya,” Sexually Transmitted Infections 96, no. 6 (2020): 457–463, 10.1136/sextrans-2019-054052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37. Nyasenu Y. T., Gbeasor‐Komlanvi F. A., Ehlan A., et al., “Prevalence and Distribution of Human Papillomavirus (HPV) Genotypes Among HIV Infected Women in Lome, Togo,” PLoS One 14, no. 2 (2019): e0212516, 10.1371/journal.pone.0212516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. Rais M., Ouyahia A., Mohammedi D., et al., “First Study of Genital HPV Infection Among Women Living With HIV Recruited From May to September 2018 in Eastern Algeria,” International Journal of STD & AIDS 34, no. 12 (2023): 9564624231179274, 10.1177/09564624231179274. [DOI] [PubMed] [Google Scholar]
  • 39. Yakub M. M., Fowotade A., Anaedobe C. G., Manga M. M., Bakare R. A., and Abimiku B. A., “Human Papillomavirus Correlates of High Grade Cervical Dysplasia Among Hiv‐Infected Women at a Major Treatment Centre in Nigeria: A Cross‐Sectional Study,” Pan African Medical Journal 33 (2019): 125, 10.11604/pamj.2019.33.125.17589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40. Aziz H., Sattar A. A., Mahmood H., Fatima S., Khurshid M., and Faheem M., “Prevalence of HPV Types in HIV‐Positive and Negative Females With Normal Cervical Cytology or Dysplasia,” Journal of Clinical Laboratory Analysis 37, no. 4 (2023): e24851, 10.1002/jcla.24851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41. Ortiz‐Gutiérrez F., Sánchez‐Minutti L., Martínez‐Herrera J. F., et al., “Identification of Genetic Variants of Human Papillomavirus in a Group of Mexican HIV/AIDS Patients and Their Possible Association With Cervical Cancer,” Polish Journal of Microbiology 70, no. 4 (2021): 501–509, 10.33073/pjm-2021-047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Abel S., Najioullah F., Voluménie J. L., et al., “High Prevalence of Human Papillomavirus Infection in HIV‐Infected Women Living in French Antilles and French Guiana,” PLoS One 14, no. 9 (2019): e0221334, 10.1371/journal.pone.0221334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43. Badial R. M., Dias M. C., Stuqui B., et al., “Detection and Genotyping of Human Papillomavirus (HPV) in HIV‐Infected Women and Its Relationship With HPV/HIV Co‐Infection,” Medicine 97, no. 14 (2018): e9545, 10.1097/MD.0000000000009545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Miguel Haddad Kury C., Santos K. C. D. S., Carestiato F. N., et al., “Human Papillomavirus Prevalence, Genomic Diversity and Related Risk Factors in Hiv‐Positive Women From a Countryside City in the State of Rio de Janeiro,” Human Vaccines & Immunotherapeutics 17, no. 3 (2021): 838–844, 10.1080/21645515.2020.1799666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45. Monteiro J. C., Fonseca R. Rd. S., Ferreira T. Cd. S., et al., “Prevalence of High Risk Hpv in Hiv‐Infected Women From Belem, Para, Amazon Region of Brazil: A Cross‐Sectional Study,” Frontiers in Public Health 9 (2021): 649152, 10.3389/fpubh.2021.649152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46. Pahwa V., Pimple S. A., Mishra G. A., and Anand K. V., “Prevalence and Determinants of Human Papilloma Virus Infection and Cervical Intraepithelial Neoplasia (CIN) Among Women Living With HIV/AIDS in Mumbai, India,” Indian Journal of Medical and Paediatric Oncology 43, no. 1 (2022): 097–102, 10.1055/s-0042-1742661. [DOI] [Google Scholar]
  • 47. Risnawati, Soejoenoes A., Hadisaputro S., et al., “HPV 52 Most Dominant Human Papillomavirus (HPV) Genotype in Women Infected by Human Immunodeficiency Virus (HIV) That Get Antiretroviral Treatment (Art,” International Journal of Pharmaceutical Research 12, no. 4 (2020): 2568–2573, 10.31838/ijpr/2020.12.04.355. [DOI] [Google Scholar]
  • 48. Boudes M., Venard V., Routiot T., Buzzi M., and Maillot F., “Prevalence and Distribution of HPV Genotypes in Immunosuppressed Patients in Lorraine Region,” Viruses 13, no. 12 (2021): 2454, 10.3390/v13122454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49. Carriero C., Fascilla F. D., Cramarossa P., Lepera A., Bettocchi S., and Vimercati A., “Colpocytological Abnormalities in HIV Infected and Uninfected Pregnant Women: Prevalence, Persistence and Progression,” Journal of Obstetrics and Gynaecology 38, no. 4 (2018): 526–531, 10.1080/01443615.2017.1373082. [DOI] [PubMed] [Google Scholar]
  • 50. Metz C. K. S., Skof A. S., Sehouli J., et al., “Assessment of High‐Risk Human Papillomavirus Infections and Cervical Dusplasia in Human Immunodeficiency Virus‐Positive Pregnany Women in Germany: A Prospective Cross‐Sectional Two Center Study,” International Journal of Gynecological Cancer 32, no. Suppl 2 (2022): A37–A38, 10.1136/ijgc-2022-ESGO.79. [DOI] [PubMed] [Google Scholar]
  • 51. Orlando G., Frati E. R., Fasolo M. M., et al., “Incident Genital HPV Infections and Potential Impact of HPV Vaccines in Adult Women Living With HIV/AIDS,” Human Vaccines & Immunotherapeutics 15, no. 7–8 (2019): 1904–1910, 10.1080/21645515.2018.1528834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52. Thorsteinsson K., Storgaard M., Katzenstein T. L., et al., “Prevalence of Cervical, Oral, and Anal Human Papillomavirus Infection in Women Living With HIV in Denmark ‐ The SHADE Cohort Study,” Journal of Clinical Virology 105 (2018): 64–71, 10.1016/j.jcv.2018.05.010. [DOI] [PubMed] [Google Scholar]
  • 53. Al‐Lawati Z., Khamis F. A., Al‐Hamdani A., et al., “Prevalence of Human Papilloma Virus in Oman: Genotypes 82 and 68 Are Dominating,” International Journal of Infectious Diseases 93 (2020): 22–27, 10.1016/j.ijid.2019.12.038. [DOI] [PubMed] [Google Scholar]
  • 54. Al Shaarani M., Lu D., Szporn A., Zakowski M., and Si Q., “Prevalence of High‐Risk HPV and Squamous Lesions in Concurrent Anal and Cervical Cytology Specimens From the Same HIV Infected Women,” Modern Pathology 33, no. 3 (2020): 321–322. [Google Scholar]
  • 55. Cameron J. E., Dennis D. C., Herrel N. R., Chapple A. G., and Hagensee M. E., “Risk of Abnormal Cervical Cytology in HIV‐Infected Women Testing Positive for Both Human Papillomavirus and Epstein‐Barr Virus in Genital Tract Specimens,” Cancer Causes & Control 31, no. 4 (2020): 365–375, 10.1007/s10552-020-01287-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56. Rodrigues L. L. S., Pilotto J. H., Martinelli K. G., 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 15, no. 6 (2023): 1328, 10.3390/v15061328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57. Biała M., Zalewska M., Szetela B., Gąsiorowski J., Leszczyszyn J., and Inglot M., “Prevalence and Genotype Distribution of Human Papillomavirus Infection Among HIV‐Infected Men Who Have Sex With Men Living in Lower Silesia, Poland,” Advances in Dermatology and Allergology 39, no. 6 (2022): 1128–1133, 10.5114/ada.2022.122607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58. Borena W., Kruis S., Kitchen M., et al., “Anal Ureaplasma Spp. Positivity Among Hiv Positive Men Who Have Sex With Men May be Associated With High‐Risk‐Type Hpv Infections,” International Journal of Infectious Diseases 84 (2019): 75–79, 10.1016/j.ijid.2019.04.025. [DOI] [PubMed] [Google Scholar]
  • 59. Bruzzesi E., Galli L., Poli A., et al., “Prevalence and Risk Factors of Anal HPV Infection in MSM Living With HIV: Identifying the Target Groups to Prioritize for Immunization,” JAIDS Journal of Acquired Immune Deficiency Syndromes 91, no. 2 (2022): 226–231, 10.1097/QAI.0000000000003057. [DOI] [PubMed] [Google Scholar]
  • 60. Callejo A., Del Mar Molina M., Dinares M. C., et al., “Exploratory Study of an Oral Screening Dysplasia Program for HIV‐Infected Men Who Have Sex With Men,” AIDS (London, England) 36, no. 10 (2022): 1383–1391, 10.1097/QAD.0000000000003287. [DOI] [PubMed] [Google Scholar]
  • 61. Giuliani M., Latini A., Colafigli M., et al., “Vaccine‐Preventable Anal Infections by Human Papillomavirus Among HIV‐Infected Men Who Have Sex With Men,” Future Microbiology 13, no. 13 (2018): 1463–1472, 10.2217/fmb-2018-0149. [DOI] [PubMed] [Google Scholar]
  • 62. Marra E., Siegenbeek Van Heukelom M. L., Leeman A., et al., “Virological and Serological Predictors of Anal High‐Grade Squamous Intraepithelial Lesions Among Human Immunodeficiency Virus‐Positive Men Who Have Sex With Men,” Clinical Infectious Diseases 68, no. 8 (2019): 1377–1387, 10.1093/cid/ciy719. [DOI] [PubMed] [Google Scholar]
  • 63. Parisi S. G., Basso M., Scaggiante R., et al., “Oral and Anal High‐Risk Human Papilloma Virus Infection in Hiv‐Positive Men Who Have Sex With Men over a 24‐Month Longitudinal Study: Complexity and Vaccine Implications,” BMC Public Health 19, no. 1 (2019): 645, 10.1186/s12889-019-7004-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64. Squillace N., Bernasconi D. P., Lapadula G., et al., “HPV 16 and 18 Contribute to Development of Anal Dysplasia in HIV Infection Irrespective of Gender and Sexual Orientation,” HIV Medicine 22, no. 9 (2021): 860–866, 10.1111/hiv.13143. [DOI] [PubMed] [Google Scholar]
  • 65. Patel P., Bush T., Kojic E. M., et al., “Prevalence, Incidence, and Clearance of Anal High‐Risk Human Papillomavirus Infection Among HIV‐Infected Men in the SUN Study,” Journal of Infectious Diseases 217, no. 6 (2018): 953–963, 10.1093/infdis/jix607. [DOI] [PubMed] [Google Scholar]
  • 66. Beliakov I., Senina M., Tyulenev Y., Novoselova E., Surovtsev V., and Guschin A., “The Prevalence of High Carcinogenic Risk of HPV Genotypes Among HIV‐Positive and HIV‐Negative MSM From Russia,” Canadian Journal of Infectious Diseases and Medical Microbiology 2021 (2021): 6641888, 10.1155/2021/6641888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67. Wang C. C., Chang S. L., Chu F. Y., Cheng C. Y., and Cheng S. H., “Human Papillomavirus Infection and Anal Cytology in Taiwanese Homosexual Men With and Without HIV Infection,” Journal of Infection in Developing Countries 13, no. 4 (2019): 318–325, 10.3855/jidc.11162. [DOI] [PubMed] [Google Scholar]
  • 68. Zhou Y., Lin Y. F., Meng X., et al., “Anal Human Papillomavirus Among Men Who Have Sex With Men in Three Metropolitan Cities in Southern China: Implications for HPV Vaccination,” Vaccine 38, no. 13 (2020): 2849–2858, 10.1016/j.vaccine.2020.02.009. [DOI] [PubMed] [Google Scholar]
  • 69. Ong J. J., Walker S., Grulich A., et al., “Incidence, Clearance, and Persistence of Anal Human Papillomavirus in Men Who Have Sex With Men Living With Human Immunodeficiency Virus: Implications for Human Papillomavirus Vaccination,” Sexually Transmitted Diseases 46, no. 4 (2019): 229–233, 10.1097/OLQ.0000000000000958. [DOI] [PubMed] [Google Scholar]
  • 70. Revollo B., Videla S., Sirera G., et al., “Natural History of Anal Squamous Intraepithelial Lesions in HIV‐Positive Men With Normal Baseline Cytology,” AIDS Patient Care and STDs 33, no. 11 (2019): 459–465, 10.1089/apc.2019.0186. [DOI] [PubMed] [Google Scholar]
  • 71. Ejaz M., Andersson S., Batool S., Ali T., and Ekström A. M., “Anal Human Papillomavirus Infection Among Men Who Have Sex With Men and Transgender Women Living With and Without HIV in Pakistan: Findings From a Cross‐Sectional Study,” BMJ Open 11, no. 11 (2021): e052176, 10.1136/bmjopen-2021-052176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72. Chinyowa S., Palefsky J. M., Chirenje Z. M., Makunike‐Mutasa R., Munjoma M., and Muguti G. I., “Anal Human Papillomavirus Infection in HIV‐Positive Men and Women at Two Opportunistic Infections Clinics in Harare, Zimbabwe,” BMC Public Health 18, no. 1 (2018): 1260, 10.1186/s12889-018-6170-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73. Hidalgo‐Tenorio C., Calle‐Gómez I., Moya‐Megías R., et al., “HPV Infection of the Oropharyngeal, Genital and Anal Mucosa and Associated Dysplasia in People Living With HIV,” Viruses 15, no. 5 (2023): 1170, 10.3390/v15051170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74. Boldrini N. A. T., Volpini L. P. B., De Freitas L. B., et al., “Anal Hpv Infection and Correlates in Hiv‐Infected Patients Attending a Sexually Transmitted Infection Clinic in Brazil,” PLoS One 13, no. 7 (2018): e0199058, 10.1371/journal.pone.0199058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75. Zhang J., Chen X., Ye Y., et al., “Increased CD4+ T Cell Count Is Associated With Lower Anal Human Papillomavirus Prevalence Among HIV‐Positive Male Cohort in Taizhou, China: A Cross‐Sectional Study,” BMC Infectious Diseases 22, no. 1 (2022): 250, 10.1186/s12879-022-07251-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76. Santinelli L., Scordio M., Frasca F., et al., “Lack of TLRS Activation in Anal Cells of HIV+ Men May Contribute to HPV Persistence,” Topics in Antiviral Medicine 29, no. 1 (2021): 173. [Google Scholar]
  • 77. Vergori A., Garbuglia A. R., Piselli P., et al., “Oral Human Papillomavirus Dna Detection in HIV‐Positive Men: Prevalence, Predictors, and Co‐Occurrence at Anal Site,” BMC Infectious Diseases 18, no. 1 (2018): 25, 10.1186/s12879-017-2937-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78. Cuba L. B., Tello A. G., and Bejarano S. C., “Anogenital Human Papillomavirus Infection Among HIV Positive Peruvian Men,” in 24th World Congress of Dermatology 2019, (2019), https://www.wcd2019milan‐dl.org/abstract‐book/assets/html/abstracts/22‐infectious‐diseases.html. [Google Scholar]
  • 79. Tsikis S., Hoefer L., Bethimoutis G., et al., “Risk Factors, Prevalence, and Site Concordance of Human Papillomavirus in High‐Risk Greek Men,” European Journal of Cancer Prevention 27, no. 5 (2018): 514–520, 10.1097/CEJ.0000000000000366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80. Chachage M., Parikh A. P., Mahenge A., et al., “High‐Risk Human Papillomavirus Genotype Distribution Among Women Living With and at Risk for HIV in Africa,” AIDS 37, no. 4 (2023): 625–635, 10.1097/QAD.0000000000003437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81. Adedimeji A., Ajeh R., Dzudie A., et al., “Cervical Human Papillomavirus DNA Detection in Women Living With HIV and HIV‐Uninfected Women Living in Limbe, Cameroon,” Journal of Clinical Virology 128 (2020): 104445, 10.1016/j.jcv.2020.104445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82. Ouladlahsen A., Fayssel N., Bensghir R., et al., “The Human Papillomavirus Among Women Living With Human Immunodeficiency Virus in Morocco A Prospective Cross‐Sectional Study,” Journal of Infection in Developing Countries 12, no. 6 (2018): 477–484, 10.3855/jidc.9711. [DOI] [PubMed] [Google Scholar]
  • 83. Teixeira M. F., Sabidó M., Leturiondo A. L., de Oliveira Ferreira C., Torres K. L., and Benzaken A. S., “High Risk Human Papillomavirus Prevalence and Genotype Distribution Among Women Infected With HIV in Manaus, Amazonas,” Virology Journal 15, no. 1 (2018): 36, 10.1186/s12985-018-0942-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84. Mchome B., Linde D. S., Manongi R., et al., “Incident Detection of Human Papillomavirus ‐ A Prospective Follow‐Up Study Among Tanzanian Women With a Focus on HIV Status,” International Journal of Infectious Diseases 110 (2021): 165–170, 10.1016/j.ijid.2021.07.011. [DOI] [PubMed] [Google Scholar]
  • 85. Jalil E. M., Wilson E. C., Monteiro L., et al., “High Prevalence of Anal High‐Risk HPV Infection Among Transwomen: Estimates From a Brazilian RDS Study,” Journal of the International AIDS Society 24, no. 3 (2021): e25691, 10.1002/jia2.25691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86. Harfouch O., Eyasu R., Cover A. A., et al., “Risk Factors for Anal Dysplasia and Linkage to HRA IN Transgender Women,” Sexual Health 19, no. 2 (2022): xiii, 10.1071/SHv19n2abs. [DOI] [Google Scholar]
  • 87. Ferré V. M., Ekouevi D. K., Gbeasor‐Komlanvi F. A., et al., “Prevalence of Human Papillomavirus, Human Immunodeficiency Virus and Other Sexually Transmitted Infections Among Female Sex Workers in Togo: a National Cross‐Sectional Survey,” Clinical Microbiology and Infection 25, no. 12 (2019): 1560.e1–1560.e7, 10.1016/j.cmi.2019.04.015. [DOI] [PubMed] [Google Scholar]
  • 88. Alberts C. J., Heard I., Canestri A., et al., “Incidence and Clearance of Anal Human Papillomavirus (HPV)‐16 and HPV‐18 Infection, and Their Determinants, Among Human Immunodeficiency Virus‐Infected Men Who Have Sex With Men in France,” Journal of infectious diseases 221, no. 9 (2020): 1488–1493, 10.1093/infdis/jiz623. [DOI] [PubMed] [Google Scholar]
  • 89. Dona M. G., Giuliani M., Rollo F., et al., “Incidence and Clearance of Anal High‐Risk Human Papillomavirus Infection and Their Risk Factors in Men Who Have Sex With Men Living With HIV,” Scientific Reports 12, no. 1 (2022): 184, 10.1038/s41598-021-03913-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90. Patel P., Bush T., Conley L., et al., “Prevalence, Incidence, and Clearance of Human Papillomavirus Types Covered by Current Vaccines in Men With Human Immunodeficiency Virus in the SUN Study,” Journal of Infectious Diseases 222, no. 2 (2020): 234–242, 10.1093/infdis/jiz425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91. Poynten I. M., Jin F., Molano M., et al., “Possible Reactivation of Latent Anal Human Papillomavirus Associated With Markers of Immune Dysfunction in Gay and Bisexual Men,” Cancer Epidemiology, Biomarkers & Prevention 31, no. 5 (2022): 1052–1057, 10.1158/1055-9965.EPI-21-1346. [DOI] [PubMed] [Google Scholar]
  • 92. Yunihastuti E., Teeratakulpisarn N., Jeo W. S., et al., “Incidence, Clearance, Persistence and Factors Related With High‐Risk Anal HPV Persistence in South‐East Asian MSM and Transgender Women,” AIDS 34, no. 13 (2020): 1933–1941, 10.1097/QAD.0000000000002654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93. Posada D. H., Acevedo L. S. T., Arredondo M. V., and Vásquez G. I. S., “High‐Risk Human Papillomavirus Infection and Associated Factors in the Anal Canal of HIV‐Positive Patients in Medellín, 2017–2018,” Revista de Saúde Pública 54 (2020): 93, 10.11606/s1518-8787.2020054001692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94. Combes J.‐D., Heard I., Poizot‐Martin I., et al., “Prevalence and Risk Factors for Anal Human Papillomavirus Infection in Human Immunodeficiency Virus‐Positive Men Who Have Sex With Men,” Journal of Infectious Diseases 217, no. 10 (2018): 1535–1543, 10.1093/infdis/jiy059. [DOI] [PubMed] [Google Scholar]
  • 95. Perez‐Quintanilla M., Mendez‐Martinez R., Vazquez‐Vega S., et al., “High Prevalence of Human Papillomavirus and European Variants of HPV 16 Infecting Concomitantly to Cervix and Oral Cavity in Hiv Positive Women,” PLoS One 15, no. 4 (2020): e0227900, 10.1371/journal.pone.0227900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96. Castillejos‐García I., Ramírez‐Amador V. A., Carrillo‐García A., García‐Carrancá A., Lizano M., and Anaya‐Saavedra G., “Type‐Specific Persistence and Clearance Rates of HPV Genotypes in the Oral and Oropharyngeal Mucosa in an HIV/AIDS Cohort,” Journal of Oral Pathology & Medicine 47, no. 4 (2018): 396–402, 10.1111/jop.12687. [DOI] [PubMed] [Google Scholar]
  • 97. Giuliani M., Rollo F., Vescio M. F., et al., “Oral Human Papillomavirus Infection in HIV‐Infected and HIV‐Uninfected Msm: The OHMAR Prospective Cohort Study,” Sexually Transmitted Infections 96, no. 7 (2020): 528–536, 10.1136/sextrans-2019-054301. [DOI] [PubMed] [Google Scholar]
  • 98. Ferre V. M., Sadio A., Gbeasor‐Komlanvi D. F., et al., “High Prevalence of HPV, Other STI, and Anal Lesions Among Msm in Togo,” Topics in Antiviral Medicine 31, no. 2 (2023): 412. [Google Scholar]
  • 99. Duan R., Zhang H., Wu A., et al., “Prevalence and Risk Factors for Anogenital HPV Infection and Neoplasia Among Women Living With HIV in China,” Sexually Transmitted Infections 98, no. 4 (2022): 247–254, 10.1136/sextrans-2021-055019. [DOI] [PubMed] [Google Scholar]
  • 100. McHome B. L., Kjaer S. K., Manongi R., et al., “Hpv Types, Cervical High‐Grade Lesions and Risk Factors for Oncogenic Human Papillomavirus Infection Among 3416 Tanzanian Women,” Sexually Transmitted Infections 97, no. 1 (2021): 56–62, 10.1136/sextrans-2019-054263. [DOI] [PubMed] [Google Scholar]
  • 101. Qiao Y. P., Wang A. L., Fang L. W., Hann K., and Wang L. H., “High‐Risk Human Papillomavirus Infection and Associated Factors Among HIV‐Positive Women in High HIV‐Burden Areas of China,” Biomedical and environmental sciences: BES 33, no. 3 (2020): 206–212, 10.3967/bes2020.029. [DOI] [PubMed] [Google Scholar]
  • 102. Conde‐Ferráez L., Chan‐Mezeta A., Gómez‐Carballo J. G., Ayora‐Talavera G., and González‐Losa M. R., “Human Papillomavirus Genotypes Infecting the Anal Canal and Cervix in HIV+ Men and Women, Anal Cytology, and Risk Factors for Anal Infection,” Pathogens 12, no. 2 (2023): 252, 10.3390/pathogens12020252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 103. Hidalgo‐Tenorio C., Gil‐Anguita C., López Ruz M. A., Omar M., López‐Hidalgo J., and Pasquau J., “ART Is Key to Clearing Oncogenic Hpv Genotypes (HR‐HPV) in Anal Mucosa of HIV‐Positive Msm,” PLoS One 14, no. 10 (2019): e0224183, 10.1371/journal.pone.0224183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104. Gupta R., Hussain S., Hariprasad R., et al., “High Prevalence of Cervical High‐Grade Lesions and High‐Risk Human Papillomavirus Infections in Women Living With HIV: A Case for Prioritizing Cervical Screening in This Vulnerable Group,” Acta Cytologica 66, no. 6 (2022): 496–506, 10.1159/000525340. [DOI] [PubMed] [Google Scholar]
  • 105. Camargo M., Del Río‐Ospina L., Soto‐De León S. C., et al., “Association of HIV Status With Infection by Multiple HPV Types,” Tropical Medicine & International Health 23, no. 11 (2018): 1259–1268, 10.1111/tmi.13142. [DOI] [PubMed] [Google Scholar]
  • 106. Cambrea S. C., Aschie M., Resul G., et al., “HPV and HIV Coinfection in Women From a Southeast Region of Romania‐PICOPIV Study,” Medicina (Kaunas, Lithuania) 58, no. 6 (2022): 760, 10.3390/medicina58060760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 107. Mandiriri A. M., Pascoe M. J., Shamu T., and Lowe S., “Cervical Human Papillomavirus Prevalence, Risk Factors and Outcomes in a Cohort of HIV‐Infected Women in Harare, Zimbabwe,” Southern African Journal of HIV Medicine 21, no. 1 (2020): a1123, 10.4102/SAJHIVMED.V21I1.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 108. Swai P., Kjaer S. K., Mchome B., et al., “The Association Between Human Papillomavirus and Cervical High‐Grade Cytology Among HIV‐Positive and HIV‐Negative Tanzanian Women: A Cross‐Sectional Study,” Acta Obstetricia et Gynecologica Scandinavica 100, no. 4 (2021): 775–785, 10.1111/aogs.14102. [DOI] [PubMed] [Google Scholar]
  • 109. Chikandiwa A., Kelly H., Sawadogo B., et al., “Prevalence, Incidence and Correlates of Low Risk HPV Infection and Anogenital Warts in a Cohort of Women Living With HIV in Burkina Faso and South Africa,” PLoS One 13, no. 5 (2018): e0196018, 10.1371/journal.pone.0196018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 110. Gupta R., Hussain S., Hariprasad R., et al., “Concurrent Cervical and Anal High‐Risk Human Papillomavirus Infection in Women Living With HIV: An Observational Case‐Control Study,” JAIDS Journal of Acquired Immune Deficiency Syndromes 91, no. 3 (2022): 319–324, 10.1097/QAI.0000000000003064. [DOI] [PubMed] [Google Scholar]
  • 111. Megersa T., Dango S., Kumsa K., Lemma K., and Lencha B., “Prevalence of High‐Risk Human Papillomavirus Infections and Associated Factors Among Women Living With HIV in Shashemene Town Public Health Facilities, Southern Ethiopia,” BMC Women's Health 23, no. 1 (2023): 125, 10.1186/s12905-023-02279-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 112. Klein K. L., Goron A. R., Taylor G., and Roque D. M., “Pap Smear Outcomes in HIV‐Positive Women >=65 Years and HIV‐Negative Matched Controls,” Gynecologic Oncology 159, no. Suppl 1 (2020): 183–184, 10.1016/j.ygyno.2020.05.280. [DOI] [Google Scholar]
  • 113. Peyyala S., Mahey R., Vashist S., Wig N., Mathur S., and Tanwar P., “A Comparative Study of Prevalence of Hpv Infection, Precancerous Lesions of Cervix and Vulva in Hivpositive and Negative Women,” Indian Journal of Gynecologic Oncology 19, no. 3 (2021): 58, 10.1007/s40944-021-00548-2. [DOI] [Google Scholar]
  • 114. Massad L. S., Xie X., Minkoff H., et al., “Longitudinal Assessment of Abnormal Papanicolaou Test Rates Among Women With HIV,” AIDS 34, no. 1 (2020): 73–80, 10.1097/QAD.0000000000002388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 115. Tosato Boldrini N. A., Bondi Volpini L. P., Freitas L. B., et al., “Sexually Transmitted Infections Among Women Living With HIV in a Brazilian City,” Brazilian Journal of Infectious Diseases 25, no. 1 (2021): 101044, 10.1016/j.bjid.2020.101044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 116. Fusco F. M., Vichi F., Bisanzi S., et al., “HPV Infection and Pre‐Neoplastic Cervical Lesions Among 321 HIV+ Women in Florence, Italy, 2006‐2016: Prevalence and Associated Factors,” New Microbiologica 41, no. 4 (2018): 268–273. [PubMed] [Google Scholar]
  • 117. Menon S., Rossi R., Benoy I., Bogers J. P., and van den Broeck D., “Human Papilloma Virus Infection in HIV‐Infected Women in Belgium: Implications for Prophylactic Vaccines Within This Subpopulation,” European Journal of Cancer Prevention 27, no. 1 (2018): 46–53, 10.1097/CEJ.0000000000000271. [DOI] [PubMed] [Google Scholar]
  • 118. Videla S., Tarrats A., Ornelas A., et al., “Incidence of Cervical High‐Grade Squamous Intraepithelial Lesions in HIV‐1‐Infected Women With No History of Cervical Pathology: Up to 17 Years of Follow‐Up,” International Journal of STD & AIDS 30, no. 1 (2019): 56–63, 10.1177/0956462418792653. [DOI] [PubMed] [Google Scholar]
  • 119. Hopkins K. L., Jaffer M., Hlongwane K. E., et al., “Assessing National Cervical Cancer Screening Guidelines: Results From an HIV Testing Clinic Also Screening for Cervical Cancer and HPV in Soweto, South Africa,” PLoS One 16, no. 7 (2021): e0255124, 10.1371/journal.pone.0255124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 120. Ndizeye Z., Vanden Broeck D., Lebelo R. L., Bogers J., Benoy I., and Van Geertruyden J.‐P., “Prevalence and Genotype‐Specific Distribution of Human Papillomavirus in Burundi According to HIV Status and Urban or Rural Residence and Its Implications for Control,” PLoS One 14, no. 6 (2019): e0209303, 10.1371/journal.pone.0209303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 121. Ogu C. O., Achukwu P. U., and Nkwo P. O., “Prevalence and Risk Factors of Cervical Dysplasia Among Human Immunodeficiency Virus Sero‐Positive Females on Highly Active Antiretroviral Therapy in Enugu, Southeastern, Nigeria,” Asian Pacific Journal of Cancer Prevention 20, no. 10 (2019): 2987–2994, 10.31557/APJCP.2019.20.10.2987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 122. Ogunsowo K., Akadri A., Odelola O., Adefuye P., Shorunmu T., and Ebili H., “Prevalence and Predictors of Squamous Intraepithelial Lesions in Human Immunodeficiency Virus Positive Women in Sagamu, Southwest Nigeria,” Journal of Public Health in Africa 13, no. 3 (2022): 11, 10.4081/jphia.2022.1858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 123. Prathima S., Sarojini, Latha B., and Ashakiran T. R., “Study of Prevalence of Abnormal Pap Smear and Its Associated Risk Factors in HIV Positive Women: A Cross‐Sectional Study,” Journal of Obstetrics and Gynecology of India 72, no. Suppl 1 (2022): 255–261, 10.1007/s13224-021-01533-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 124. Shin S. S., Carpenter C. L., Ekstrand M. L., et al., “Cervical Cancer Awareness and Presence of Abnormal Cytology Among HIV‐Infected Women on Antiretroviral Therapy in Rural Andhra Pradesh, India,” International journal of STD & AIDS 30, no. 6 (2019): 586–595, 10.1177/0956462419825950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 125. Wang Q., Ma X., Zhang X., et al., “Human Papillomavirus Infection and Associated Factors for Cervical Intraepithelial Neoplasia in Women Living With HIV in China: A Cross‐Sectional Study,” Sexually Transmitted Infections 95, no. 2 (2019): 140–144, 10.1136/sextrans-2018-053636. [DOI] [PubMed] [Google Scholar]
  • 126. Karani L. W., Musyoki S., Orina R., Nyamache A. K., Khayeka‐Wandabwa C., and Nyagaka B., “Human Papillomavirus Genotype Profiles and Cytological Grades Interlinkages in Coinfection With HIV,” Pan African Medical Journal 35 (2020): 67, 10.11604/pamj.2020.35.67.21539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 127. Bouassa R. S. M., Belec L., Gubavu C., et al., “High Prevalence of Anal and Oral High‐Risk Human Papillomavirus in Human Immunodeficiency Virus‐Uninfected French Men Who Have Sex With Men and Use Preexposure Prophylaxis,” Open Forum Infectious Diseases 6, no. 9 (2019): ofz291, 10.1093/ofid/ofz291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 128. Clark E., Chen L., Dong Y., et al., “Veteran Women Living With Human Immunodeficiency Virus Have Increased Risk of Human Papillomavirus (HPV)‐Associated Genital Tract Cancers,” Clinical Infectious Diseases 72, no. 9 (2021): e359–e366, 10.1093/cid/ciaa1162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 129. Rositch A. F., Levinson K., Suneja G., et al., “Epidemiology of Cervical Adenocarcinoma and Squamous Cell Carcinoma Among Women Living With Human Immunodeficiency Virus Compared With the General Population in the United States,” Clinical Infectious Diseases 74, no. 5 (2022): 814–820, 10.1093/cid/ciab561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 130. Nakisige C., Adams S. V., Namirembe C., et al., “Multiple High‐Risk HPV Types Contribute to Cervical Dysplasia in Ugandan Women Living With HIV on Antiretroviral Therapy,” JAIDS Journal of Acquired Immune Deficiency Syndromes 90, no. 3 (2022): 333–342, 10.1097/QAI.0000000000002941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 131. Ye Y., Burkholder G. A., Wiener H. W., et al., “Comorbidities Associated With Hpv Infection Among People Living With HIV‐1 in the Southeastern US: A Retrospective Clinical Cohort Study,” BMC Infectious Diseases 20, no. 1 (2020): 144, 10.1186/s12879-020-4822-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 132. Shiojiri D., Mizushima D., Takano M., et al., “Anal Human Papillomavirus Infection and Its Relationship With Abnormal Anal Cytology Among MSM With or Without HIV Infection in Japan,” Scientific Reports 11, no. 1 (2021): 19257, 10.1038/s41598-021-98720-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 133. Bushara O., Weinberg S. E., Finkelman B. S., et al., “The Effect of Human Immunodeficiency Virus and Human Papillomavirus Strain Diversity on the Progression of Anal Squamous Intraepithelial Lesions,” Human Pathology 128 (2022): 20–30, 10.1016/j.humpath.2022.06.025. [DOI] [PubMed] [Google Scholar]
  • 134. Finkelman B., Weinberg S., Obeng R., Sun L., Liao J., and Yang G. Y., “HIV Infection and Low CD4 Count Are Associated With Faster Progression of HPV Mediated Anal Squamous Intraepithelial Lesions: A Large Clinicopathologic Cohort Study,” Laboratory Investigation 101, no. SUPPL 1 (2021): 410–411, 10.1038/s41374-021-00556-y. [DOI] [Google Scholar]
  • 135. Ortiz A. P., Engels E. A., Nogueras‐González G. M., et al., “Disparities in Human Papillomavirus‐Related Cancer Incidence and Survival Among Human Immunodeficiency Virus‐Infected Hispanics Living in the United States,” Cancer 124, no. 23 (2018): 4520–4528, 10.1002/cncr.31702. [DOI] [PubMed] [Google Scholar]
  • 136. Waters A. V., Dorsey K. A., Allston A., Woods A., Furness B. W., and Doshi R. K., “Risk Factors for Human Papillomavirus‐Associated Cancers Among People Living With HIV in Washington, District of Columbia,” AIDS Research and Human Retroviruses 39, no. 4 (2023): 195–203, 10.1089/AID.2022.0128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 137. Chaussade H., Le Marec F., Coureau G., et al., “Incidence of Lung and Human Papilloma Virus‐Associated Malignancies in HIV‐Infected Patients,” AIDS 36, no. 5 (2022): 665–673, 10.1097/QAD.0000000000003152. [DOI] [PubMed] [Google Scholar]
  • 138. Furukawa S., Uota S., Yamana T., et al., “Distribution of Human Papillomavirus Genotype in Anal Condyloma Acuminatum Among Japanese Men: The Higher Prevalence of High Risk Human Papillomavirus in Men Who Have Sex With Men With HIV Infection,” AIDS Research and Human Retroviruses 34, no. 4 (2018): 375–381, 10.1089/aid.2017.0197. [DOI] [PubMed] [Google Scholar]
  • 139. Kremer W., van Zummeren M., Heideman D., et al., “HPV16‐related Cervical Cancers and Precancers Have Increased Levels of Host Cell Dna Methylation in Women Living With HIV,” International Journal of Molecular Sciences 19, no. 11 (2018): 3297, 10.3390/ijms19113297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 140. Tawe L., MacDuffie E., Narasimhamurthy M., et al., “Human Papillomavirus Genotypes in Women With Invasive Cervical Cancer With and Without Human Immunodeficiency Virus Infection in Botswana,” International Journal of Cancer 146, no. 6 (2020): 1667–1673, 10.1002/ijc.32581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 141. Lin C., Franceschi S., and Clifford G. M., “Human Papillomavirus Types From Infection to Cancer in the Anus, According to Sex and Hiv Status: a Systematic Review and Meta‐Analysis,” Lancet Infectious Diseases 18, no. 2 (2018): 198–206, 10.1016/S1473-3099(17)30653-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 142. King E. M., Oomeer S., Gilson R., et al., “Oral Human Papillomavirus Infection in Men Who Have Sex With Men: A Systematic Review and Meta‐Analysis,” PLoS One 11, no. 7 (2016): e0157976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 143. Marais D. J., Passmore J. A. S., Denny L., Sampson C., Allan B. R., and Williamson A. L., “Cervical and Oral Human Papillomavirus Types in HIV‐1 Positive and Negative Women With Cervical Disease in South Africa,” Journal of Medical Virology 80, no. 6 (2008): 953–959, 10.1002/jmv.21166. [DOI] [PubMed] [Google Scholar]
  • 144. Wei F., Gaisa M. M., D'Souza G., et al., “Epidemiology of Anal Human Papillomavirus Infection and High‐Grade Squamous Intraepithelial Lesions in 29 900 Men According to Hiv Status, Sexuality, and Age: A Collaborative Pooled Analysis of 64 Studies,” Lancet HIV 8, no. 9 (2021): e531–e543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 145. Stier E. A., Clarke M. A., Deshmukh A. A., et al., “International Anal Neoplasia Society's Consensus Guidelines for Anal Cancer Screening,” International Journal of Cancer 154, no. 10 (2024): 1694–1702. [DOI] [PubMed] [Google Scholar]
  • 146. Kutz J.‐M., Rausche P., Gheit T., Puradiredja D. I., and Fusco D., “Barriers and Facilitators of Hpv Vaccination in Sub‐Saharan Africa: A Systematic Review,” BMC Public Health 23, no. 1 (2023): 974, 10.1186/s12889-023-15842-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 147. Poljak M., Šterbenc A., and Lunar M. M., “Prevention of Human Papillomavirus (HPV)‐Related Tumors in People Living With Human Immunodeficiency Virus (HIV),” Expert Review of Anti‐Infective Therapy 15, no. 11 (2017): 987–999. [DOI] [PubMed] [Google Scholar]
  • 148. Yang M., Du J., Lu H., Xiang F., Mei H., and Xiao H., “Global Trends and Age‐Specific Incidence and Mortality of Cervical Cancer From 1990 to 2019: An International Comparative Study Based on the Global Burden of Disease,” BMJ Open 12, no. 7 (2022): e055470, 10.1136/bmjopen-2021-055470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 149. Pinheiro M., Gage J. C., Clifford G. M., et al., “Association of HPV35 With Cervical Carcinogenesis Among Women of African Ancestry: Evidence of Viral‐Host Interaction With Implications for Disease Intervention,” International Journal of Cancer 147, no. 10 (2020): 2677–2686, 10.1002/ijc.33033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 150. Okoye J., Chukwukelu C., Okekpa S., Ogenyi S., Onyekachi‐Umah I., and Ngokere A., “Racial Disparities Associated With the Prevalence of Vaccine and Non‐Vaccine HPV Types and Multiple HPV Infections Between Asia and Africa: A Systematic Review and Meta‐Analysis,” Asian Pacific Journal of Cancer Prevention 22, no. 9 (2021): 2729–2741, 10.31557/apjcp.2021.22.9.2729. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supporting information.

JMV-97-e70274-s001.docx (1.4MB, docx)

Data Availability Statement

Data for this manuscript was from published studies, all of which have been cited appropriately in text and tables.

Articles from Journal of Medical Virology are provided here courtesy of Wiley

RESOURCES