Background: Infection with high-risk (HR) human papillomavirus (HPV) is associated with penile cancer in men, cervical cancer in women, and anal cancer and certain types of head and neck cancers in both sexes. Few studies have assessed the prevalence and type distribution of HPV among men in sub-Saharan Africa, where the rates of HIV and penile and cervical cancer are high.
Material and Methods: We used data from a cross-sectional study among 1813 men in Tanzania. Penile samples were tested using Hybrid Capture 2, and genotyping was done by the INNO-LiPA HPV Genotyping Extra test. Blood samples were tested for HIV. The overall and type-specific prevalence and 95% confidence interval of HPV was estimated in relation to age and HIV status.
Results: The overall prevalence of HPV was 20.5% (95% confidence interval, 18.7–22.4), the most prevalent HR HPV types being HPV52, HPV51, HPV16, HPV18, HPV35, and HPV66. The HR HPV prevalence was significantly higher in HIV-positive men (25.7%) than in HIV-negative men (15.8%; P = 0.0027). The prevalence of HPV16, HPV18 and multiple HR HPVs tended to be higher among HIV-positive men (statistically nonsignificant), whereas no differences were observed for the other HPV types.
Conclusions: We found a high prevalence of HPV types 52, 51, 16, 18, 35, and 66. This information is of relevance in the understanding of HPV type distributions across populations. Although the prevalence of HPV16 and HPV18 was slightly higher among HIV-positive men, our results indicate that HIV status does not strongly influence the distribution of HPV types. Therefore, the currently available HPV vaccines could prevent HPV infection independently of HIV status.
The overall prevalence of human papillomavirus (HPV) was 20.5%, with the most prevalent high-risk HPV types being HPV52, HPV51, HPV16, HPV18, and HPV35. There was a tendency toward a higher prevalence of HPV16 and HPV18 among HIV-positive men.
From the *Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark; †Department of Experimental Virology, Universitaetsklinikum, Tuebingen, Germany; ‡Division of Cancer Prevention, Ocean Road Cancer Institute, Dar es Salaam, United Republic of Tanzania; §Department of Obstetrics and Gynecology, Odense University Hospital, Odense, Denmark; and ¶Gynecologic Clinic, Rigs hospitalet, University of Copenhagen, Copenhagen, Denmark
Supported by Merck (ClinicalTrials.gov ID NCT00932009). The study sponsors had no role in study design, data analysis, data interpretation, writing of the report, or the decision to submit the manuscript for publication.
S.K.K. received lecture fees, advisory board fees, and research grants from Merck and Sanofi Pasteur MSD through her institution. C.M. received lecture fees and travel granted from Merck and Sanofi Pasteur MSD. T.I. received speaker honoraria from Gen-Probe GmbH, Hologic GmbH, and Roche Diagnostics GmbH. For the remaining authors, no conflicts of interest were declared.
Correspondence: Susanne Krüger Kjaer, MD, DMSC, Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen Ø, Denmark. E-mail: firstname.lastname@example.org.
Received for publication November 13, 2012, and accepted February 28, 2013.
Human papillomavirus (HPV) is the most common sexually transmitted infection worldwide. Infection with certain types of high-risk (HR) HPV is associated with penile cancer in men; cervical, vaginal, and vulvar cancer in women; and certain types of head and neck cancer, anal cancer, and genital warts in both sexes.1 There has been a growing interest in studying HPV among men because of the HPV-related disease burden in men and the risk of transmission of HPV to women.2 The distribution of HPV types may not be uniform worldwide, and therefore, characterization of HPV in different regions of the world is important. Still few studies have examined the prevalence and type distribution of HPV among men worldwide3,4 and even less among men in sub-Saharan Africa,4 where the rates of penile and cervical cancer are among the highest worldwide.5 In women, the HPV prevalence increases strongly in the years after first intercourse, and thereafter, it decreases with older age. In men, the age pattern has been less consistent, with a relatively flat HPV prevalence curve in some studies and peak HPV prevalence generally not concentrated in the younger age groups.2,4
The HIV epidemic in sub-Saharan Africa possibly exacerbates the burden of HPV-related cancers.6 An understanding of the prevalence and type distribution of HPV in sub-Saharan Africa may be of relevance in deciding the composition of future polyvalent HPV vaccines targeting a wider range of HR HPV types and can help inform vaccine policy within a given country. Here, we examine the overall and type-specific prevalence of HPV among men in Tanzania, both in relation to age and in relation to HIV status.
MATERIALS AND METHODS
We used data from a cross-sectional study called “TaMas—Tanzanian male study” conducted in an urban (Dar es Salaam region) and a rural setting (Pwani, Tanga, and Kilimanjaro regions) in Tanzania between February and June 2009. For the urban setting, men employed at two different factories and one public university were invited to participate in the study, and for the rural setting, men visiting their sick relatives at different public health facilities were invited to participate. We aimed at including a total sample of 2000 men. In total, we managed to enroll 1933 men in the study.
The study was approved by the National Health Research Ethics Review Committee of the National Institute of Medical Research in Tanzania. Informed consent was obtained from all study participants. Each study participant received approximately US $5 for their time and inconvenience.
A structured questionnaire was used to collect sociodemographic and lifestyle characteristics. Subsequently, the participants underwent a clinical examination with specimen collection. At the examination, circumcision status was assessed, and cases of genital warts were diagnosed. Material for HPV testing from the penis was collected using 2 prewetted (saline) Dacron swabs: one from the glans penis and the preputial cavity in uncircumcised men or the coronal sulcus in circumcised men, respectively, and one from the shaft and the corpus of the penis. The penile swabs were placed in one tube containing 1 mL Digene specimen transport medium (Digene Corporation, Gaithersburg, MD) for later HPV testing. Subsequently, the suspended specimens were stored at −20°C and shipped at the end of the study to the Department of Experimental Virology, Tuebingen University in Germany for HPV testing.
The specimens were tested for the presence of HPV by the Hybrid Capture 2 (HC2) method (Qiagen, Hildesheim, Germany) using an HR probe detecting 13 HR HPV types (HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68) and a low-risk (LR) probe detecting 5 LR HPV types (HPV types 6, 11, 42, 43, and 44). We used the Food and Drug Administration recommended cutoff value for test-positive results of 1.0 or more relative light units/Co (equivalent to 1 pg HPV DNA per 1 mL of sampling buffer).
The HC2-positive samples were analyzed for specific genotypes using the polymerase chain reaction (PCR)–based assay INNO-LiPA HPV Genotyping Extra test (LiPA) (Innogenetics Inc, Gent, Belgium). LiPA is a line probe assay, based on the reverse hybridization principle, designed for the identification of 18 HR HPV genotypes (HPV types 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 73, and 82) as well as 7 LR HPV genotypes (HPV types 6, 11, 40, 43, 44, 54, and 70) and 3 types with undefined risk (HPV types 69, 71, and 74). Genotyping was performed on 200 μL of the remaining denatured product from the HC2 test. DNA was isolated using the MagnaPure device (Roche Systems, Indianapolis, IN). Subsequently 5 μL of DNA solution was used for the LiPAV Extra SPF-PCR assay. Polymerase chain reaction products were then denatured, and a 10-μL aliquot was hybridized to a HPV Genotype detection strip. The resulting strip reading was performed using a scanner, the LiRAS prototype software (Innogenetics Inc).
HC2-positive samples where no HPV was detected using LiPA were classified as “LiPA negative” (n = 5), HC2-positive samples where the strip was not interpretable because of the presence of too many reactive probe lines were classified as “LiPA fail” (n = 40), and finally, samples that were LiPA positive but where no specific HPV type could be identified or where the LiPA test could not discriminate between 2 HPV types were classified as HPV of undetermined type (“HPV X”) (n = 10).
All study participants were offered to have a blood sample taken to be tested for HIV. HIV counseling was offered both before and after HIV testing according to national and international guidelines. Blood samples were tested according to the World Health Organization–approved HIV serial testing algorithm,7 which is in accordance with the Tanzanian Ministry of Health guidelines. Initially, one rapid immunoassay was used (SD Bioline HIV-1/2 3.0 rapid test; Standard Diagnostics Inc, Giheung-ku, Republic of South Korea), and if positive, an additional confirmatory immunological test (Determine HIV-1/2 test; Abbott Laboratories SA, Johannesburg, South Africa) was performed. If there was discrepancy between these two tests, a third test was used (UNIGold method/Recombigen HIV; Trinity Biotech, Jamestown, NY). The results of the test were given to each participant individually in a separate room to ensure confidentiality. Men testing positive for HIV were referred to an HIV care and treatment clinic and were offered a thorough follow-up, with determination of primary CD4 cell level, advice, information, and psychological support. Immediate treatment was offered when relevant. The follow-up was voluntary and free of charge.
We examined the sociodemographic characteristics (age at study entry, educational level, marital status, religion, urban/rural setting) of the study population.
The overall and type-specific prevalence of HPV and 95% confidence intervals (CIs) were estimated among the total study population and in relation to age at study entry (≤19, 20–24, 25–29, 30–34, 35–39, 40–49, and ≥50 years). The type-specific prevalence of HPV was also estimated among HPV-positive men. Furthermore, the overall and type-specific HPV prevalence was estimated in relation to HIV status (HIV positive, HIV negative, not tested). Men who refused to be tested for HIV but reported to be HIV positive in the questionnaire (n = 30) were categorized as HIV positive, and men tested for HIV but with missing values on HIV result (n = 20) were categorized as not tested for HIV.
We performed tests for trend examining the association between age at study entry and the prevalence of HPV and HIV, respectively, using logistic regression with age at study entry as a continuous variable. χ2 Tests were used for the comparison of two proportions. All analyses were performed using the statistical software SAS version 9.2.
In total, 1933 men participated in the study. We excluded men with no information on age at study entry (n = 5) and men with penile samples with insufficient volume or quality for HPV testing (n = 115), leaving 1813 men for the analyses.
Sociodemographic Characteristics of the Study Population
In Table 1, sociodemographic characteristics of the study population are displayed. In all, 917 men (50.7%) were from urban areas and 893 men (49.3%) from rural areas in Tanzania. The median age at study entry was 30 years (mean, 34.2 years), with 18.1% being 24 years or younger, whereas 25.4% were 40 years or older. Almost 14% of men had no formal education, whilst 34% had completed primary school. Most men participating in the study were either Muslims (49.2%) or Catholics (31.0%). A total of 1671 men (92.4%) reported ever to have had a female sexual partner. The median age at first sexual intercourse was 19 years, and the median number of lifetime sexual partners was 6. In total, 1594 men (88.1%) were circumcised (data not shown).
Overall, Type-Specific, and Age-Specific Prevalence of HPV
A total of 372 men (20.5%; 95% CI, 18.7–22.4) were HPV positive by HC2 (HR and/or LR). Among these, 5 samples were LiPA negative; for 40 samples, the LiPA test failed; and for 10 samples, no specific HPV type could be identified (HPV X), leaving 317 men with a result from the LiPA test.
The overall prevalence of HC2 HR HPV was 16.2% (95% CI, 14.5–17.9), and that of LR HPV was 9.9% (95% CI, 8.5–11.3) (Table 2). The prevalence of HPV (HR and/or LR) increased from 12.2% (95% CI, 4.7–19.6) in the youngest age group to 25.0% (95% CI, 19.2–30.8) in the oldest age group (Fig. 1A) in the total study population. This increase was statistically significant (P = 0.0054).
In the total study population, the most prevalent HR HPV types were HPV52 (5.8%; 95% CI, 4.7–6.9), HPV51 (4.8%; 95% CI, 3.8–5.8), HPV16 (2.6%; 95% CI, 1.9–3.3), HPV18 (2.5%; 95% CI, 1.8–3.2), and HPV35 (2.3%; 95% CI, 1.6–3.0). Furthermore, we found a high prevalence of HPV66 (4.1%; 95% CI, 3.2–5.0). The prevalence of the specific HR HPV types followed the same age pattern as the overall prevalence of HPV.
The most prevalent LR HPV types were HPV6 (2.6%; 95% CI, 1.9–3.3) and HPV11 (2.0%; 95% CI, 1.3–2.6). In addition, we found a high prevalence of HPV70 (2.9%; 95% CI, 2.1–3.6) and HPV74 (2.2%; 95% CI, 1.5–2.9). Again, the age-specific prevalence of LR HPV types followed the same pattern as the overall prevalence of HPV.
The prevalence of multiple (≥2) HR HPV was 8.4% (95% CI, 7.1–9.7) in the total study population and 48.0% (95% CI, 42.5–53.5) among HPV-positive men (Table 2).
HPV Prevalence and Type Distribution in Relation to HIV Status
In total, 140 men (7.7%) tested HIV positive and 330 men (18.2%; 95% CI, 16.4–20.0) refused to be tested for HIV. Among men tested for HIV, the overall prevalence of HIV was 9.4% (95% CI, 8.0–10.9). The prevalence of HIV was 1.9% (95% CI, 0.0–5.6) in the youngest age group and 14.7% (95% CI, 9.2–20.3) in the oldest age group (Fig. 1A). This increase was statistically significant (P < 0.0001).
The overall prevalence of HPV was significantly higher among HIV-positive (35.0%; 95% CI, 27.1–42.9) compared with HIV-negative men (20.0%; 95% CI, 17.8–22.1) (P < 0.0001) and men who refused to be tested for HIV (16.7%; 95% CI, 12.7–20.7) (Table 3). The prevalence of HR HPV was also highest among HIV-positive men (25.7%; 95% CI, 18.5–33.0) compared with HIV-negative men (15.8%; 95% CI, 13.8–17.7) (P = 0.0027), and so was the prevalence of LR HPV (HIV-positive men: 25.7%; 95% CI, 18.5–33.0; HIV-negative men: 8.9%; 95% CI, 7.3–10.4) (P < 0.0001; data not shown).
In HIV-positive men, the prevalence of HPV (HR and/or LR) increased from 21.7% (95% CI, 4.9–38.6) in 25- to 29-year-olds to 52.2% (95% CI, 31.8–72.6) in the oldest age group (Fig. 1B). This increase was statistically significant (P = 0.0120). In HIV-negative men, there was no statistically significant increase in the prevalence of HPV by age (P = 0.1899): the prevalence of HPV (HR and/or LR) was 17.3% (95% CI, 7.0–27.6) in the youngest age group and 21.1% (95% CI, 14.1–28.0) in the oldest age group (Fig. 1C).
The prevalence of HPV16 tended to be higher in HIV-positive men (21.4%; 95% CI, 9.0–33.8) than in HIV-negative men (12.3%; 95% CI, 8.1–16.6); however, this difference was not statistically significant (P = 0.1160). Similarly, we found a tendency toward a higher prevalence of HPV18 among HIV-positive men (21.4%; 95% CI, 9.0–33.8) compared with HIV-negative men (12.3%; 95% CI, 8.1–16.6) (P = 0.1160). We found no differences in the prevalence of other HR or LR HPV types in relation to HIV status.
Finally, the prevalence of multiple HR HPV was higher in HIV-positive (57.1%; 95% CI, 42.2–72.1) than among HIV-negative men (45.4%; 95% CI, 38.9–51.9), although the difference did not reach statistical significance (P = 0.1605) (Table 3).
To our knowledge, this is the first study to report HPV DNA prevalence and type distribution of HPV in relation to HIV status among men in Tanzania. We found an overall HPV prevalence of 20.5%. Previous studies conducted among men in sub-Saharan Africa reported HPV prevalence estimates ranging between 26.5% and 50.0%.8–10 It is, however, difficult to compare those studies because of the heterogeneity between the studies with regard to age distribution in the different study populations. The difference in the estimates of HPV prevalence may also be caused by differences in sexual behavior, that is, number of sexual partners or differences in the proportion of HIV-positive and the proportion of circumcised men, which both are well-known risk determinants of HPV infection among men. The overall HIV prevalence in our study was 9.4% (95% CI, 8.0–10.9), which is in agreement with the HIV prevalence in the Dar es Salaam region in Tanzania (>7.4%) as reported by United Nations Programme on HIV/AIDS.11
In women, there is often a peak in the prevalence of HPV after sexual debut followed by a decline because most infections clear and new sexual encounters decrease.12 In contrast, the age pattern in men has been less consistent in various studies. Among men in Tanzania, we found an increase in the prevalence of HPV with age. Other studies, conducted primarily in HIV-negative men, reported a relatively flat HPV prevalence curve in men.2,4 This association was apparent in HIV-negative men in our study, as well; however, in HIV-positive men, the prevalence of HPV increased substantially with age. In contrast, Tobian et al.13 found that among HIV-positive men, the prevalence of HPV was high (>70%) in all age groups. The different age pattern in men and women is possibly explained by differences in the epithelial lining of the penis and the cervix. The keratinized epithelium on the penis does not as easily allow the immune system to get in contact with the HPV infection, implying a less efficient acquired immune response in men.
The most prevalent HR HPV types were HPV types 52, 51, 16, 18, 35, and 66 among men in Tanzania. This is in agreement with previous studies among men in sub-Saharan Africa.8,10 We have previously reported a similar pattern among women in Tanzania, the most common HR HPV types being HPV52 (4.4%) and HPV16 (3.8%).14 Likewise, a recent meta-analysis of HPV prevalence among women showed that HPV52 was particularly frequent in Africa (2.4% vs. Europe 0.4%).15 In line with our finding, other studies among men in sub-Saharan Africa have reported a relatively high prevalence of HPV52 ranging between 2.5% and 9.6%.8,10,16,17 Human papillomavirus type 52 belongs to the alpha 9 species group, together with HPV16, and is thus considered an important HR HPV type in carcinogenesis to humans.18 Nonetheless, HPV16 and HPV18 account for the largest number of HPV-related cancers worldwide: HPV16 and HPV18 are the most common HPV types in penile cancer and cervical cancer,19,20 and furthermore, HPV16 is the most common HR HPV type detected in head and neck cancers.21
The prevalence of multiple HR HPV types in the present study was 8.4% in the total study population, and approximately half of HPV-positive men had multiple types. It is still not clear whether infection with multiple HPV types interferes, either directly or immunologically, with the persistence of a given HPV type or with progression.22,23 Some studies have found that infection with multiple HPV types, both in men24 and in women,25 is associated with HPV persistence.
In keeping with previous studies,13,26 we found a significantly higher prevalence of HPV among HIV-positive men compared with HIV-negative men. This could suggest that immune suppression in HIV-positive men leads to increased acquisition and reduced clearance of HPV,6 possibly increasing the risk of progression to cancer. This finding could explain the high rates of penile and cervical cancer in sub-Saharan Africa5 and underlines the importance of the implementation of HPV vaccines in sub-Saharan Africa. Nevertheless, our data are cross sectional, and the association found could also imply that HPV infection increases the risk of becoming HIV positive, as suggested by other studies.27,28
Few studies have assessed the HPV type distribution in relation to HIV status in men: Tobian et al.13 found a higher prevalence of HPV16, HPV18, and other HPV types among HIV-positive men compared with HIV-negative men in Uganda. We found a slightly higher (statistically nonsignificant) prevalence of HPV16 and HPV18 among HIV-positive compared with HIV-negative men in Tanzania, although no difference in the type distribution of other HR or LR HPV types in relation to HIV status. We have previously demonstrated that among women in Tanzania, there was no difference in the type distribution of HPV in relation to HIV status.14
This study provides important information about the prevalence of HPV among men in Tanzania. The strengths of this study are the large sample size, a wide age range, and a relatively large proportion of HIV-positive men, resulting in greater statistical power to examine the association between HIV and HPV. The study also has some limitations that should be acknowledged. The cross-sectional design does not allow for assessment of persistence of HPV infection, an important predictor of progression to cancer,29–31 and we could not determine the timing of acquisition of HPV and HIV. We used a nonrandom convenience sample; possibly, this could imply that our sample may not be representative of the general male population in Tanzania. We excluded 115 men with penile samples inadequate for HPV testing, and it is unknown how those would have contributed to the overall prevalence of HPV in this population. Finally, only the samples that were HC2 positive were tested by LiPA, and owing to differences between the HPV genotypes included in HC2 and LiPA, the prevalence of some HPV types that do not cross react to the HC2 HR and LR probe32 may be underestimated.
In conclusion, we found a high prevalence of HPV types 52, 51, 16, 18, 35, and 66. This information is of relevance in the understanding of HPV type distributions across populations. No statistically significant difference in HPV types was seen among HIV-negative and HIV-positive men, although the prevalence of HPV16 and HPV18 was slightly higher among HIV-positive men. However, because these HPV types are already included in the current HPV vaccines, our results indicate that the vaccines could prevent HPV infection independently of HIV status.
1. IARC. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Volume 90: Human Papillomaviruses. Lyon, France: International Agency for Research on Cancer, 2007.
2. Giuliano AR, Lazcano-Ponce E, Villa LL, et al. The human papillomavirus infection in men study: Human papillomavirus prevalence and type distribution among men residing in Brazil, Mexico, and the United States. Cancer Epidemiol Biomarkers Prev 2008; 17: 2036–2043.
3. Dunne EF, Nielson CM, Stone KM, et al. Prevalence of HPV infection among men: A systematic review of the literature. J Infect Dis 2006; 194: 1044–1057.
4. Smith JS, Gilbert PA, Melendy A, et al. Age-specific prevalence of human papillomavirus infection in males: A global review. J Adolesc Health 2011; 48: 540–552.
5. Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010; 127: 2893–2917.
6. Tobian AA, Kigozi G, Gravitt PE, et al. Human papillomavirus incidence and clearance among HIV-positive and HIV-negative men in sub-Saharan Africa. AIDS 2012; 26: 1555–1565.
7. Joint United Nations Programme on HIV/AIDS (UNAIDS)–WHO. Revised recommendations for the selection and use of HIV antibody tests. Wkly Epidemiol Rec 1997; 72: 81–87.
8. Veldhuijzen NJ, Dhont N, Vyankandondera J, et al. Prevalence and concordance of HPV, HIV, and HSV-2 in heterosexual couples in Kigali, Rwanda. Sex Transm Dis 2012; 39: 128–135.
9. Muller EE, Chirwa TF, Lewis DA. Human papillomavirus (HPV) infection in heterosexual South African men attending sexual health services: Associations between HPV and HIV serostatus. Sex Transm Infect 2010; 86: 175–180.
10. Ng’ayo MO, Bukusi E, Rowhani-Rahbar A, et al. Epidemiology of human papillomavirus infection among fishermen along Lake Victoria Shore in the Kisumu District, Kenya. Sex Transm Infect 2008; 84: 62–66.
12. Schiffman M, Castle PE, Jeronimo J, et al. Human papillomavirus and cervical cancer. Lancet 2007; 370: 890–907.
13. Tobian AA, Grabowski MK, Kigozi G, et al. High-risk human papillomavirus prevalence is associated with HIV infection among heterosexual men in Rakai, Uganda. Sex Transm Infect 2013; 89: 122–127.
14. Dartell M, Rasch V, Kahesa C, et al. Human papillomavirus prevalence and type distribution in 3603 HIV-positive and HIV-negative women in the general population of Tanzania: The PROTECT study. Sex Transm Dis 2012; 39: 201–208.
15. Bruni L, Diaz M, Castellsague X, et al. Cervical human papillomavirus prevalence in 5 continents: Meta-analysis of 1 million women with normal cytological findings. J Infect Dis 2010; 202: 1789–1799.
16. Smith JS, Backes DM, Hudgens MG, et al. Prevalence and risk factors of human papillomavirus infection by penile site in uncircumcised Kenyan men. Int J Cancer 2010; 126: 572–577.
17. Auvert B, Lissouba P, Cutler E, et al. Association of oncogenic and nononcogenic human papillomavirus with HIV incidence. J Acquir Immune Defic Syndr 2010; 53: 111–116.
18. Schiffman M, Herrero R, Desalle R, et al. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005; 337: 76–84.
19. Miralles-Guri C, Bruni L, Cubilla AL, et al. Human papillomavirus prevalence and type distribution in penile carcinoma. J Clin Pathol 2009; 62: 870–878.
20. Munoz N, Bosch FX, Castellsague X, et al. Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer 2004; 111: 278–285.
21. Kreimer AR, Clifford GM, Boyle P, et al. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: A systematic review. Cancer Epidemiol Biomarkers Prev 2005; 14: 467–475.
22. Moscicki AB, Ellenberg JH, Farhat S, et al. Persistence of human papillomavirus infection in HIV-infected and -uninfected adolescent girls: Risk factors and differences, by phylogenetic type. J Infect Dis 2004; 190: 37–45.
23. Schiffman M, Kjaer SK. Chapter 2: Natural history of anogenital human papillomavirus infection and neoplasia. J Natl Cancer Inst Monogr 2003; 31: 14–19.
24. Kjaer SK, Munk C, Winther JF, et al. Acquisition and persistence of human papillomavirus infection in younger men: A prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomarkers Prev 2005; 14: 1528–1533.
25. Ho GY, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998; 338: 423–428.
26. Mbulawa ZZ, Coetzee D, Marais DJ, et al. Genital human papillomavirus prevalence and human papillomavirus concordance in heterosexual couples are positively associated with human immunodeficiency virus coinfection. J Infect Dis 2009; 199: 1514–1524.
27. van der Loeff MF, Nyitray AG, Giuliano AR. HPV vaccination to prevent HIV infection: Time for randomized controlled trials. Sex Transm Dis 2011; 38: 640–643.
28. Tobian AA, Grabowski MK, Kigozi G, et al. Human papillomavirus clearance in men is associated with HIV acquisition and increased foreskin dendritic cell density in Rakai, Uganda. J Infect Dis 2013. [Epub ahead of print].
29. Kjaer SK, van den Brule AJ, Paull G, et al. Type specific persistence of high risk human papillomavirus (HPV) as indicator of high grade cervical squamous intraepithelial lesions in young women: Population based prospective follow up study. BMJ 2002; 325: 572.
30. Koshiol J, Lindsay L, Pimenta JM, et al. Persistent human papillomavirus infection and cervical neoplasia: A systematic review and meta-analysis. Am J Epidemiol 2008; 168: 123–137.
31. Cuschieri KS, Cubie HA, Whitley MW, et al. Persistent high risk HPV infection associated with development of cervical neoplasia in a prospective population study. J Clin Pathol 2005; 58: 946–950.
© Copyright 2013 American Sexually Transmitted Diseases Association
32. Iftner T, Villa LL. Chapter 12: Human papillomavirus technologies. J Natl Cancer Inst Monogr 2003; 31: 80–88.