Artigos

Prevalence of and risk factors for penile infection by high-risk human papillomavirus among men infected with HIV

Prevalence of and risk factors for penile infection by high-risk human papillomavirus among men infected with HIV

Running head: Genital HPV in men infected with HIV

Giuseppe Figliuolo1,2, Jusimara Maia1, Alex P. Jalkh1, Angélica E. Miranda3, Luiz C. L. Ferreira1

  1. Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Manaus, Amazonas, Brazil
  2. Universidade Estadual do Amazonas, Manaus, Amazonas, Brazil
  3. Universidade Federal do Espírito Santo, Vitória, Espírito Santo, Brazil

Correspondence to:

Giuseppe Figliuolo

Rua 08, n° 28-B, Apt 1104, Edifício Napolis Conjunto Parque Tropical, Parque 10

CEP: 69055-747

Tel/ FAX.: 55(92)36321846

E-mail: gf_urol@hotmail.com

Abstract

This study aimed to determine the prevalence of and risk factors for high-risk human papillomavirus (HPV) genital infection and precursor lesions of penile cancer among patients infected with human immunodeficiency virus (HIV). In total, 276 men with a mean age of 34.6 years were included. All participants were subjected to peniscopic examination under magnification, collection of genital exfoliated cells for detecting HPV types using Hybrid Capture, and biopsy surgery of clinically observable lesions and aceto-white areas for histopathological studies. The prevalence of high-risk HPV types was 43%. Penile lesions were present in 85/276 participants (27%), of which genital warts were the most common (25/85; 29%). HIV-positive (HIV+) men with CD4+ T-cell counts Keywords: HPV; Male gender; HIV; Peniscopy; Hybrid Capture

INTRODUCTION

The human papillomavirus causes a broad clinical spectrum of epithelial tumours, ranging from benign anogenital warts to anogenital cancer. Most cases of anal and cervical cancer and the majority of basaloid penile cancer and warts are associated with HPV (Muñoz et al., 2003; Gross and Pfister, 2004; Palefsky, 2006). The high-risk HPV genotypes 16 and 18 are associated with most anogenital cancers and are observed more frequently in genital warts and low-grade dysplasia than the low-risk HPV strains 6 and 11 (Muñoz et al., 2003).
Penile cancer is rarely seen in developed countries. Between 1973 and 2002, the annual incidence of primary malignant penile cancer in the United States was 0.69/100 000 males (Barnholtz-Sloan et al., 2007). Penile cancer is a frequent disorder in Brazil; according to the world ranking of disease incidence, Brazil ranks second behind the continent of Africa (Datasus, 2011). Penile cancer represents 2% of all male cancers in Brazil and is more frequent in the north and northeast than in the south and southeast regions of the country, according to the Brazilian National Institute of Cancer (INCA, 2009).
Individuals with HIV/AIDS have a higher risk than uninfected individuals of developing cancer caused by HPV (Frisch et al., 2001; Clifford et al., 2005; Grulich et al., 2007) and have a higher incidence of and more persistent HPV infections (Palefsky, 2006; Palefsky and Holly, 2003; Harris et al., 2005; Strickler et al., 2005; Cameron and Hagensee, 2007). The incidence of HPV-associated cancers is also increased in transplant patients and other immunosuppressed individuals (Grulich et al., 2007; Cameron and Hagensee, 2007). HIV progressively destroys local cellular immunity through infection of CD4+ T-cells and Langerhans cells in the skin (Chopra and Tyring, 1997). In turn, chronic HPV infection may exacerbate the pathogenesis of HIV by inducing inflammatory cytokine production (Gage et al., 2000).

This study aimed at determining the prevalence of penile lesions and penile infections with high-risk HPV types among Brazilian men infected with HIV. The risk factors associated with genital HPV infection were also evaluated.

Abstract

This study aimed to determine the prevalence of and risk factors for high-risk human papillomavirus (HPV) genital infection and precursor lesions of penile cancer among patients infected with human immunodeficiency virus (HIV). In total, 276 men with a mean age of 34.6 years were included. All participants were subjected to peniscopic examination under magnification, collection of genital exfoliated cells for detecting HPV types using Hybrid Capture, and biopsy surgery of clinically observable lesions and aceto-white areas for histopathological studies. The prevalence of high-risk HPV types was 43%. Penile lesions were present in 85/276 participants (27%), of which genital warts were the most common (25/85; 29%). HIV-positive (HIV+) men with CD4+ T-cell counts

Keywords: HPV; Male gender; HIV; Peniscopy; Hybrid Capture

INTRODUCTION

The human papillomavirus causes a broad clinical spectrum of epithelial tumours, ranging from benign anogenital warts to anogenital cancer. Most cases of anal and cervical cancer and the majority of basaloid penile cancer and warts are associated with HPV (Muñoz et al., 2003; Gross and Pfister, 2004; Palefsky, 2006). The high-risk HPV genotypes 16 and 18 are associated with most anogenital cancers and are observed more frequently in genital warts and low-grade dysplasia than the low-risk HPV strains 6 and 11 (Muñoz et al., 2003).

Penile cancer is rarely seen in developed countries. Between 1973 and 2002, the annual incidence of primary malignant penile cancer in the United States was 0.69/100 000 males (Barnholtz-Sloan et al., 2007). Penile cancer is a frequent disorder in Brazil; according to the world ranking of disease incidence, Brazil ranks second behind the continent of Africa (Datasus, 2011). Penile cancer represents 2% of all male cancers in Brazil and is more frequent in the north and northeast than in the south and southeast regions of the country, according to the Brazilian National Institute of Cancer (INCA, 2009).

Individuals with HIV/AIDS have a higher risk than uninfected individuals of developing cancer caused by HPV (Frisch et al., 2001; Clifford et al., 2005; Grulich et al., 2007) and have a higher incidence of and more persistent HPV infections (Palefsky, 2006; Palefsky and Holly, 2003; Harris et al., 2005; Strickler et al., 2005; Cameron and Hagensee, 2007). The incidence of HPV-associated cancers is also increased in transplant patients and other immunosuppressed individuals (Grulich et al., 2007; Cameron and Hagensee, 2007). HIV progressively destroys local cellular immunity through infection of CD4+ T-cells and Langerhans cells in the skin (Chopra and Tyring, 1997). In turn, chronic HPV infection may exacerbate the pathogenesis of HIV by inducing inflammatory cytokine production (Gage et al., 2000).

This study aimed at determining the prevalence of penile lesions and penile infections with high-risk HPV types among Brazilian men infected with HIV. The risk factors associated with genital HPV infection were also evaluated.

MATERIALS AND METHODS

This was a cross-sectional study of men aged 18 years and older who were infected with HIV and were without psychiatric disorders. Patients attending the Tropical Medicine Foundation of Amazonas in Manaus, AM, Brazil in 2010 were invited to participate in this study and gave written informed consent. The Ethical Committee for Research of the Tropical Medicine Foundation of Amazonas approved all of the procedures. All patients were interviewed and completed a standard questionnaire. Demographic, epidemiological, and clinical data were collected. All patients underwent a urologic physical examination and a peniscopy with 5% acetic acid.

Peniscopic examination

Participants were asked to remain in a supine position for the penis and scrotum examination. Exfoliated cells were collected by rubbing a wet cytobrush over the entire surface of the prepuce, the balanopreputial sulcus, the fossa navicularis, and the glans of the penis. The tip of the cytobrush was placed in 350 µl specimen transport medium (STM; Digene, São Paulo, Brazil). The peniscopic examination was performed using a magnifying lens. The penis was wrapped for 10 minutes in gauze soaked in 5% acetic acid. Some lesions, such as warts, were macroscopically visible prior to application of acetic acid, and additional aceto-white lesions became visible under magnification after application of acetic acid. Biopsies were taken from clinically visible lesions and aceto-white areas.

Histopathological evaluation

The specimens were fixed in 10% formalin-buffered solution, paraffin-embedded, sectioned, and subjected to standard haematoxylin and eosin staining. Similarities between cervical and anal squamous intraepithelial lesions and penile intraepithelial neoplasia were established via microscopy, based on the definitions of precursor neoplastic lesions described previously (Abramowitz et al., 2007; Colecchia et al., 2010). A single pathologist evaluated all of the biopsies.
The Hybrid Capture test (Qiagen, Hilden, Germany) was used to detect high-risk genital HPV types (Eleutério el al., 2010). The Qiagen test (HC2 high-risk HPV DNA test) includes probes for high-risk HPV strains 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68 (Goldstone et al., 2012). HPV types were also detected via PCR, using a previously established protocol (Oliveira et al., 2003) that uses consensus primers MY09/11 to detect a 450-base pair fragment of the L1 gene (Manos et al., 1989).

Statistical analysis

The data were entered into the Epi InfoTM electronic platform version 6.04, and statistical analysis was conducted using Statistical Package for Social Sciences® (SPSS) software version 16.0 (IBM, Armonk, NY, USA). Pearson’s chi-squared test was used with Yates’ correction when appropriate. Fisher’s exact test was applied for categorical variables when values were less than 5. Odds ratios and corresponding 95% confidence intervals were calculated. Variables with a p value of ≤0.1 were entered into the multivariate logistic regression model. For this study, p values of ≤0.05 were considered significant.

RESULTS

A total of 276 (96%) HIV-infected men were included in the study. The mean age was 34.6 years and the prevalence of high-risk HPV types was 43%. The sociodemographic characteristics of the participants are shown in Table 1. Lower education level and mulatto ethnicity were associated with high-risk HPV types.

The distribution of high-risk HPV infection according to sexual behaviour and history of sexually transmitted diseases is shown in Table 2. High-risk HPV types were more prevalent among heterosexual and bisexual men than among homosexual men. Table 3 describes the frequency of high-risk HPV infection according to HIV-related characteristics. High-risk HPV types were highly prevalent in the immunocompromised men (

Multivariate logistic regression analysis showed that high-risk HPV types were associated with mulatto ethnicity (OR = 2.51, 95% CI: 1.38–4.54), lower education level (OR = 1.89, 95% CI: 1.15–3.13), illicit drug use (OR = 1.80, 95% CI: 1.03–3.14), heterosexual orientation (OR = 2.12, 95% CI: 1.30–3.47), symptomatic AIDS (OR = 2.80, 95% CI: 1.65–4.77), AIDS-associated opportunistic infections (OR = 2.92, 95% CI: 1.78–4.78), HAART use (OR = 2.91, 95% CI: 1.78–4.77), and CD4+ T-cell count 1 biopsy.

The histopathological study revealed that 27 individuals had premalignant lesions, as shown in Table 5. Of these, 2 lesions were epidermodysplasia verruciformis. Four participants had penile intraepithelial neoplasia grade 3, 18 had intraepithelial neoplasia grade 1, 3 had bowenoid papulosis, and 1 had multiple lesions (2 bowenoid papulosis lesions and 1 penile intraepithelial neoplasia grade 1 lesion). High-risk HPV types were present in 21 (78%) of the 27 individuals. Most of the individuals with premalignant lesions (59%) had CD4+ T-cell counts

DISCUSSION

HPV is the most common sexually transmitted virus. Several studies have reported a genital HPV infection prevalence in males of 30% to 60% (Baldwin et al., 2004; Weaver et al., 2004; Kjaer et al., 2005). The prevalence of high-risk penile HPV types in the present study was 43%. Many studies, in particular those that collected exfoliated cells from the anorectal region, have suggested that the prevalence of HPV in men who have sex with men may be as high as 95% (reviewed in Palefsky, 2009). This variation in HPV prevalence among studies may be attributed to differences in sexual behaviour and age distribution in the study populations, the methods used for detection of HPV type, and the method and sites of genital cell collection.
In this study, heterosexual and bisexual men showed higher rates of infection with high-risk genital HPV types than homosexual men. This is likely because of the higher rate of HPV infection among women in the study region (Corrêa, 2005). Castellsagué et al. also found a higher prevalence of HPV infection (40%) in men with a lower education level than in those with a higher education level (19.5%) (Castellsagué et al., 2002).

The prevalence of high-risk genital HPV types was significantly higher among patients with AIDS, carriers of opportunistic diseases, and patients with low CD4+ T-cell counts. This is consistent with other studies showing that immunocompromised individuals have a higher risk of HPV infection, including pre-invasive or invasive lesions in the anogenital region (Dilner et al., 2000; Scott et al., 2001; Hagensee et al., 2004).

Approximately 30% of histopathological diagnosis unrelated to HPV infection in aceto-white lesions was found in this study, probably because peniscopy has a high rate of false-positive results. The appearance of aceto-white and infectious lesions were likely to be secondary to nonspecific inflammatory processes, post-coital traumas, or cytological material collection (Shultz and Skelton, 1988; Griffiths et al., 1991).

In this study, 27 (10%) of the HIV-infected men presented with penile lesions, and 21 (78%) of them were associated with high-risk HPV types. HPV DNA has been observed in 70% to 100% of penile intraepithelial neoplasias and in 29% to 81% of penile invasive cancers. HPV type 16 is the most prevalent (Aynaud et al., 1998; Dilner et al., 2000). Few reports concerning the study of penile intraepithelial neoplastic or invasive cancer in HIV-infected men exist (Gomousa-Michael et al., 2000; Frish et al., 2001; Porter et al., 2002; Grulich et al., 2007; Kreuter et al., 2008). Kreuter at al. (2008) observed a prevalence of penile and anal intraepithelial neoplasia of 4.2% and 59.3%, respectively, in 263 HIV-infected homosexual men. In the present study, most of the HIV-infected men presenting with penile lesions had low CD4+ T-cell counts (

Some limitations of this study must be acknowledged. A sectional study cannot analyse the effects of high-risk genital HPV types in patients infected with HIV. This issue is best addressed by prospective studies. Given the low prevalence of some risk factors in this patient sample, it is possible that the number of patients studied was insufficient to detect a statistical association between some independent variables and high-risk HPV types. The possibility of biased answers cannot be ruled out because of the general tendency to give socially acceptable replies in face-to-face interviews.

It is important to discuss the use of HPV vaccines in this group. The 2 available vaccines have not yet been demonstrated to show efficacy in young people infected with HIV. Several trials are ongoing to determine if HPV vaccines are effective in HIV-infected men and women (Heard, 2011). The frequency of HPV-related cancers is not expected to decline. Although penile and anal cancers are uncommon, their incidence has increased in HIV-infected homosexual men in the HAART era (Shiels et al., 2011). Thus, implementation of vaccines could be an excellent strategy to reduce the incidence. The impact of screening and treating high-grade penile or anal intraepithelial neoplasias to prevent penile and anal cancer is not easy to determine and has not yet been proven cost-effective (Kane, 2012).

The diagnosis and treatment of males with HPV-associated lesions, especially immunocompromised patients, may help identify individuals at high risk for developing penile cancer and would be an important step in halting the spread of sexually transmitted diseases.

REFERENCES

Abramowitz L, Benabderrahmane D, Ravaud P, Walker F, Rioux C, Jestin C. 2007. Anal squamous intraepithelial lesions and condyloma in HIV-infected heterosexual men, homosexual men and women: prevalence and associated factors. AIDS 21:1457–1465.

Aynaud O, Piron D, Barraso R, Poveda JD. 1998. Comparison of clinical, histological, and virological symptoms of HPV in HIV-1 infected men and immunocompetent subjects. Sex Transm Infect 74:32–34.
Baldwin S, Wallace D, Papenfuss M, Abrahamsen M, Vaught LC, Giuliano AR. 2004. Condom use and other factors affecting penile human papillomavirus detection in men attending a sexually transmitted disease clinic. Sex Transm Dis 31:601–607.

Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR. 2007. Incidence trends in primary malignant penile cancer. Urol Oncol 25:361–367.

Cameron JE, Hagensee ME. 2007. Human papillomavirus infection and disease in the HIV+ individual. Cancer Treat Res 133:185–213.

Castellsagué X, Bosch FX, Muñoz N, Shah KV. 2002. Environmental co-factors in HPV carcinogenesis. Virus Res 89:191–199.

Colecchia M, Nicolai N, Paolini B, and Salvioni R. 2010. Pre-cancerous penile lesions. European Urological Review 5:23–26.

Corrêa GJ. 2005. Prevalência do Papilomavírus Humano (HPV) em mulheres portadoras de lesões intra-epiteliais escamosas de alto grau e carcinoma epidermóide invasor de colo uterino. Tese (Mestrado).

Fundação de Medicina Tropical do Amazonas.

Chopra KF, Tyring SK. 1997. The impact of the human immunodeficiency virus on the human papillomavirus epidemic. Arch Dermatol 133:629–633.

Clifford GM, Polesel J, Smith JS, Rickenbach M. 2005. Cancer risk in the Swiss HIV Cohort Study: associations with immunodeficiency, smoking, and highly active antiretroviral therapy. J Natl Cancer Inst 97:425–432.

Datasus. Banco de dados do Sistema Único de Saúde. 2009 (acesso em 21 mai 2011). Disponível em: http://datasus.gov.br

Dillner J, von Krogh G, Horenblas S, Meijer CJ. 2000. Etiology of squamous cell carcinoma of the penis. Scand J Urol Nephrol 205:189–193.

Eleutério J Jr, Barros IC, Cavalcante DI, Eleutério RM, Giraldo PC. 2010. HPV-DNA hybrid capture test: influence of cellularity in penile samples. Acta Cytol 54:546–550.

Frisch M, Biggar RJ, Engels EA, Goedert JJ. 2001. Association of cancer with AIDS-related immunosuppression in adults. J Amer Med Assoc 285:1736–1745.

Instituto Nacional do Câncer (INCA). Ministério da Saúde. 2009. Estimativas 2008-2009: incidência do Câncer no Brasil (acesso em 23 mar de 2009). Disponível em: http: //www.inca.gov.br/estimativa/2009.

Gage JR, Sandhu AK, Nihira M, Bonecini-Almeida MG, Cristoforoni P, Kishimoto T, Montz FJ, Martinez-Maza O. 2000. Effects of human papillomavirus-associated cells on human immunodeficiency virus gene expression. Obstet Gynecol 96:879–885.

Gomousa-Michael M, Gialama E, Gomousas N, Gialama G. 2000. Genital human papillomavirus infection and associated penile intraepithelial neoplasia in males infected with the human immunodeficiency virus. Acta Cytol 44:305–309.

Goldstone SE, Lowe B, Rothmann T, Nazarenko I. 2012. Evaluation of the hybrid capture 2 assay for detecting anal high-grade dysplasia. Int J Cancer 131:1641–1648.

Gross G, Pfister H. 2004. Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts. Med Microbiol Immunol 193:35–44.

Griffths M, Penna LK, Barrasso R, Tovey SJ. 1991. Aceto-white change of the glans penis associated with balanitis not human papillomavirus infection. Int J STD AIDS 2:211–212.

Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. 2007. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 370:59–67.

Hagensee ME, Cameron JE, Leigh JE, Clark RA. 2004. Human papillomavirus infection and disease in HIV-infected individuals. Am J Med Sci 328:57–63.

Harris TG, Clark RA, Burk RD, Palefsky JM. 2005. Incidence of cervical squamous intraepithelial lesions associated with HIV serostatus, CD4 cell counts, and human papillomavirus test results. J Amer Med Assoc 293:1471–1476.

Heard I. 2011. Human papillomavirus, cancer and vaccination. Curr Opin HIV AIDS 6:297–302.

Kane MA. 2012. Preventing cancer with vaccines: progress in the global control of cancer. Cancer Prev Res (Phila) 5:24–29.

Kjaer SK, Munk C, Winther JF, Jorgensen HO, Meijer CJ, Van Den Brule AJ. 2005. Acquisition and persistence of human papillomavirus infection in younger men: a prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomarkers Prev 14:1528–1533.

Kreuter A, Brockmeyer NH, Weissenborn SJ, Gambichler T, Stucker M, Altmeyer P. 2008. Penile intraepithelial neoplasia is frequent in HIV-positive men with anal dysplasia. J Invest Dermatol 128:2316–2324.

Manos MM, Ting Y, Wright DK, Lewis AJ, Broker TR, Wolinsky SM. 1998. The use of polymerase chain reaction amplification for the detection of genital human papillomavirus. Cancer Cells 7:209–214.

Muñoz N, Bosch FX, De Sanjose S, Herrero R, Castellsagué X, Shah KV. 2003. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348:518–527.

Oliveira LHS, Rodrigues EVM, Lopes APTS, Fernandes AP, Cavalcanti SMB. 2003. HPV 16 detection in cervical lesions, physical state of viral DNA and changes in p53 gene. São Paulo Med J 121:67–71.

Palefsky JM. 1998. Human papillomavirus infection and anogenital neoplasia in human immunodeficiency virus-positive men and women. J Natl Cancer Inst Monogr 23:15–20.

Palefsky JM. 2006. Human papillomavirus-related tumors in HIV. Curr Opin Oncol 18:463–468.

Palefsky JM. 2009. Human papillomavirus-related disease in people with HIV. Curr Opin HIV AIDS 4:52–56.

Porter WM, Francis N, Hawkins D, Dinneen M, Bunker CB. 2002. Penile intraepithelial neoplasia: clinical spectrum and treatment of 35 cases. Br J Dermatol 147:1159–1165.

Schultz RE, Skelton HG. 1998. Value of acetic acid screening for flat genital condylomata in men. J Urol 140:1431–1444.

Scott M, Nakagawa M, Moscicki AB. 2001. Cell-mediated immune response to human papillomavirus infection. Clin Diagn Lab Immunol 18:209–20.

Shiels MS, Pfeiffer RM, Gail MH, Hall HI, Li J, Chaturvedi AK. 2011. Cancer burden in the HIV-infected population in the United States. J Natl Cancer Inst 103:753–762.

Strickler HD, Burk RD, Fazzari M, Anastos K, Minkoff H, Massad LS. 2005. Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. J Natl Cancer Inst 97:577–586.

Sun XW, Kuhn L, Ellerbrock TV, Chiasson MA, Bush TJ, Wright TC, Jr. 1997. Human papillomavirus infection in women infected with the human immunodeficiency virus. N Engl J Med 337:1343–1349.

Weaver BA, Feng Q, Holmes KK, Kiviat N, Lee SK, Meyer C. 2004. Evaluation of genital sites and sampling techniques for detection of human papillomavirus DNA in men. J Infect Dis 15:677–685.

Table 1. Sociodemographic characteristics of men infected with HIV according to the status of genital infection with high-risk HPV types (n = 276)

CharacteristicsHPV+ N (%)p value
Age
18–29 years
30–49 years
≥50 years
47 (47%)
68 (45%)
5 (21%)
0.0626*
Race/Colour
Mulatto
White
Black
Asian
101 (50%)
11 (24%)
7 (39%)
1 (25%)
0.0032**
Marital status
Single
Married
Cohabiting
Divorced/separated
Widowed
68 (43%)
19 (36%)
26 (47%)
6 (86%)
1 (50%)
0.1318**
Education
≤8 years
9–11 years
>12 years
Illiterate
52 (54%)
49 (39%)
18 (35%)
1 (50%)
0.0167**
Drug use
Yes
No
36 (55%)
84 (40%)
0.0528*
Cigarette Smoking
Yes
No
36 (48%)
84 (42%)
0.4300*
*Pearson’s chi-square test
**Fisher’s exact test

Table 2. Distribution of high-risk HPV infection according to sexual behaviour and history of sexually transmitted diseases

FactorsHPV+ (%)p value
Sexual orientation
Homosexual
Heterosexual
Bisexual

33 (33%)
59 (55%)
28 (41%)

0.0039*
Nº of partners in the last year
0
1
2–9
≥10
11 (46%)
45 (46%)
40 (43%)
24 (46%)
0.8082*
Condom use before HIV+ status
Sometimes
Always
Never
97 (42%)
5 (72%)
18 (46%)
0.3134**
Condom use after HIV+ status
No sexual relations
Sometimes
Always
Never
19 (54%)
14 (50%)
85 (41%)
2 (29%)
0.3690**
History of STDs
Yes
No
83 (47%)
37 (37%)
0.1605*
*Pearson’s chi-square test (significance p ≤ 0.05)
**Fisher’s exact test (significance p ≤ 0.05)
STDs, sexually transmitted diseases

Table 3. Distribution of genital infection with high-risk HPV types according to HIV-related factors

FactorsHPV+ (%)p value
Time since HIV diagnosis¹
≤3 years
4–6 years
7–9 years
≥10 years
86 (44%)
18 (47%)
6 (40%)
10 (40%)
0.9337*
Opportunistic diseases76 (57%)
44 (31%)
Yes
No
76 (57%)
44 (31%)
<0.0001*
Use of HAART2
Yes
No
79 (52%)
41 (33%)
0.0168*
Time on HAART
<1 year
1–2 years
2–3 years
>3 years
46 (59%)
11 (69%)
3 (25%)
19 (43%)
0.0666*
CD4+ T-cell count³
<200
200–349
350–500
>500
62 (60%)
27 (40%)
14 (34%)
6 (15%)
<0.0001*
Viral load4
Undetectable
<30,000
>30,000
Upper threshold (>500,000)
27 (40%)
42 (39%)
37 (53%)
3 (75%)
0.1684**
Phase of HIV infection¹
AIDS
Viral carrier
93 (52%)
27 (27%)
0.0002*
1. A total of 276 participants in the study.
2. A total of 152 participants using HAART.
3. A total of 252 participants with CD4 T-cell results
4. A total of 251 participants with viral load results.
*Pearson’s chi-square test.
**Fisher’s exact test.

Note: WHAT ARE OPPORTUNISTIC INFECTIONS?

HIV-related opportunistic infections:

Herpes zoster

Mucocutaneous herpes simplex

Viral meningoencephalitis

Pulmonary tuberculosis

Extrapulmonary tuberculosis (lymph node and extra lymph node)

Atypical mycobacteriosis

Cytomegalovirus

Pulmonary and extrapulmonary cryptococcosis

Chronic intestinal cryptosporidiosis

Chronic intestinal isosporidium

Neurocryptococcosis

Neurotoxoplasmosis

Progressive multifocal leukoencephalopathy

Reactivation of Chagas disease

Exacerbation of skin diseases (psoriasis, seborrhoeic dermatitis, onychomycosis, extensive complicated dermatophytoses, oral leukoplakia)

Recurrent genital candidiasis

Oral and oesophageal candidiasis

Candidosis of trachea, bronchi, or lungs

Pneumocystosis

Chronic diarrhoea

Viral and bacterial pneumonias

Lymphomas (Hodgkin’s disease and non-Hodgkin’s lymphoma, cerebral primary lymphoma)

Invasive cervical cancer

Recurrent sepsis by bacteria of salmonella type (non-typhoid)

Kaposi’s sarcoma

Disseminated histoplasmosis

Table 4. Independent factors associated with high-risk HPV types following multivariate logistic regression analysis

FactorsAdjusted OR*95% CI**p value
Race/Colour
Mulatto vs. other2.511.38–4.540.0032

Level of education
≤8 years vs. >8 years1.891.15–3.130.0167
Drug use
Yes vs. no1.801.03–3.140.0528
Sexual orientation
Other (bisexual + heterosexual) vs. homosexual2.12

1.30–3.470.0039
AIDS vs. latent HIV infection2.80

1.65–4.77 0.0002
Opportunistic diseases
Yes vs. no2.921.78–4.78
<0.0001
On HAART
Yes vs. no2.911.78–4.770.0168
CD4+ T-cell count
<200 vs. ≥2003.311.84–5.96<0.0001
*OR = Odds ratio, **95% CI = 95% confidence intervals

Table 5. Histopathological findings in patients with a positive peniscopy

Histopathological lesionsN(%)
Angiokeratoma
Chronic nonspecific balanitis
Nonspecific ulcerative balanitis
Chronic nonspecific balanoposthitis
Condylomata acuminata
Condylomata plana
Epidermodysplasia
Nonspecific chronic eczema
Hypermelanosis
Intraepithelial neoplasia grade 3
Fungal infection
Lichen sclerosus
Lichen planus
Intraepithelial neoplasia grade 1
Molluscum contagiosum
Melanocytic nevus
Bowenoid papulosis
Postite chronic nonspecific
No significant changes
Total number of samples examined
1
2
1
2
19
1
2
1
1
4
1
2
1
18
6
1
5
1
6
75
1
2
1
2
27
1
2
1
1
6
1
2
1
25
9
1
7
1
9
100