Penile HPV prevalence and associated factors among 20–70-year-old men in Sri Lanka: A Study in a Lower&amp; Middle-Income Country

doi:10.21203/rs.3.rs-5318516/v1

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Penile HPV prevalence and associated factors among 20–70-year-old men in Sri Lanka: A Study in a Lower& Middle-Income Country

https://doi.org/10.21203/rs.3.rs-5318516/v1

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Background

Human papillomavirus (HPV) is the most common sexually transmitted infection globally. Each year, persistent High Risk (HR) HPV infection causes 69,400 cancers in males, with a rising incidence across the world. While contributing significantly to the disease burden in men and plays a crucial role in transmitting the infection to women. Estimating male HPV genotype prevalence and associated factors is crucial for developing effective HPV preventive strategies.

Method

A community-based descriptive-cross-sectional study was conducted to estimate the penile HPV prevalence and identify the significant associated factors for HPV infection among 20–70-year-old clinically normal men in Sri Lanka. Multi-stage probability proportionate cluster sampling was done to recruit a sample of 579 study subjects. The chi-square test was used with a significance level of p < 0.05, and bivariate analysis followed by multivariate (logistic regression) analysis was conducted to explore possible determinants of HPV infection and calculate adjusted Odds Ratios (OR).

Results

Penile HPV genotype prevalence for any genotype was 5.7% (n = 33, 95% CI:3.9–7.9) and HR genotype prevalence was 1.7% (n = 10 ,95% CI: 0.3–3.1) among clinically normal men. Identified HR HPV genotypes were HPV-59 (n = 4), HPV-16 (n = 3), HPV-45 (n = 2) and HPV-33 (n = 1) however, HPV-18 was not detected. The significant associated factors for HPV infection were having > 1 female partner/s lifetime (p = 0.02) (Adjusted OR, 2.4,95%CI:1.1–4.9) and having sexual relationships being unmarried (p = 0.04) (Adjusted OR, 3.5,95% CI:1.04–12.1).

Conclusion

Human papillomavirus is a DNA virus that can cause abnormal tissue growth and is considered the most prevalent sexually transmitted infection (STI) globally(1). Among over 200 different HPV genotypes that have been identified, more than 40 genotypes can be transmitted through sexual contact and cause anogenital mucosal tumours(2). Sexually transmitted genotypes are classified into Low-Risk (LR) and HR while the HR genotypes are associated with potential malignancies(3). Approximately 69,400 HPV-driven cancers have occurred among males in a year globally over the past few decades with an increasing trend. The HPV DNA was identified in around 88% of anal cancers, 50% of oropharyngeal cancers, and 30–50% of penile cancers (4)(5).

HPV immunization efforts in most LMICs have primarily focused on women, despite men also being carriers of HPV infection(6). Preventing HPV infection among males in LMICs is crucial for reducing male HPV-driven male cancer burden and female HPV transmission, as 90% of the cervical cancer burden exists in these regions(7). This could help accelerate progress toward the global goal of cervical cancer elimination by 2102, particularly in light of setbacks from the COVID-19 pandemic, as endorsed by the 73rd World Health Assembly(8). However, community-based data on male HPV prevalence is limited and shows wide regional differences, with a global pooled prevalence of 31% for any HPV genotype and 21% for high-risk HPV genotype(1). In Sri Lanka, females aged 20–59 had a cervical prevalence of 3.3% for any HPV genotype, with 1.2% having HR HPV genotypes(9).The prevalence of HPV among males had not been estimated in Sri Lanka. Therefore, this study aimed to determine penile HPV prevalence, and prevalence of different HPV genotypes, and associated factors for HPV infection. These findings are crucial for developing comprehensive public health strategies targeting HPV-driven cancer prevention in Sri Lanka.

The study was conducted in the District of Gampaha in Sri Lanka from 2022 to 2023 among clinically normal sexually active men aged 20 to 70 years, who had resided in the district for more than 6 months prior to the study. Exclusions were made for individuals with diagnosed sexual dysfunction, physical disabilities hindering penetrative sexual activities, or psychiatric illnesses impairing questionnaire responses. A prevalence estimate of 50% was used to calculate the maximum sample size and a design effect of 1.5 was applied, resulting in an adjusted sample size of 640. Using multistage cluster sampling 32 clusters were selected, ensuring representation from rural and urban areas. A cluster size of 20 was chosen based on feasibility and previous experience with HPV prevalence studies among females in Sri Lanka(9). An interviewer-administered questionnaire was used for data collection. The questionnaire was validated with concurrent validity, content validity, face and convergent validity. All participants were recruited at the field level by 6 trained study coordinators who were male Public Health Inspectors (PHII) and interviewed by 6 trained interviewers (medical officers) in the clinic setting. Six (6) teams were formed including 1 coordinator PHI and 1 medical officer (MO) and clusters were allocated to each team based on geographic feasibility for data and sample collection. Eligible participants were recruited according to numbers identified for each age category and an informed written consent was obtained at the field level by the coordinator. After obtaining consent an appointment card was issued with a reference number, and referred to attend the identified clinic for medical examination, data and specimen collection. The administration of the questionnaire and specimen collection at the clinic was conducted on the same day or the next day after cluster recruitment. Intra-rater reliability of the questionnaires and test-retest reliability were tested using the Kappa statistics.

The HPV detection was done by PCR testing using the primers GP5+/GP6 + for HPV DNA detection, considering the acceptance of the high sensitivity of HPV DNA detection(10)(11). The reliability of laboratory procedures was assessed using the Kappa statistics. Known HPV-positive specimens and known HPV-negative specimens as negative control were tested initially for HPV DNA by selected method for PCR using GP5+/GP6 + primers. Further, negative and positive controls were included in each batch of specimens tested to ensure the validity of the test.

Data was entered, processed, and analyzed using SPSS version 23rd version. The association of socio-demographic factors and the presence of contributory factors (medical, surgical, and sexual behavioural) for acquiring HPV infection among study participants followed by factors of regular sexual partner was assessed. The Chi-square test was used as the main test of significance. Fisher’s exact test was used whenever the expected values were small. The independent variables for the model were selected from factors with a significant value of less than 0.25 (P < 0.25) in the bivariable analysis, which were associated with HPV infection. The multivariate (logistic regression) analysis was carried out to explore possible determinants of HPV infection accounting for confounding and assess the relationship. Ethical clearance was obtained from the Post Graduate Institute of Medicine Colombo (PGIM) Ethical Review Committee, Colombo, and the research ethics review committee of the WHO regional office for South-East Asia (‎SEARO-ERC). Informed written consent was secured before the study. All measures were taken to minimize risk and maximize benefits. Participation was voluntary, with the option to withdraw at any time without penalty or loss of medical care. Clinically normal men refer to men who do not present any signs or symptoms of disease or abnormalities upon medical examination. Ever married was defined as both married legally or customary.

Most of the study sample were Sinhalese (96.5%) while a small percentage were Tamils (2.1%) Muslims (1%). The majority was Buddhists (80.1%), most (47.3%) completed General Certificate of Education (GCE) Ordinary Level (O/L) and 25.2% completed GCE Advanced Level (A/L). Almost 55.8% consumed tobacco products and 80% consumed alcohol at a variable frequency. However, the majority (92.4%) never consumed any illegal drugs in their lifetime. None of the participants received HPV vaccination.

Characteristic	HPV Positive (%)	HPV Negative (%)	p-value OR & (95%CI)
Marital status
Never married	9.1	24.5	p = 0.04*
Married**	90.9	75.5	OR = 3.25(0.98–10.83)
History of anogenital wart
Yes	0	3.3	Not applicable
No	100	96.7
History of phimosis
Yes	6.1	5.1	p = 0.81*
No	93.9	94.9	OR = 1.19(0.27–5.24)
History of circumcision
Yes	6.1	4	p = 0.57*
No	93.9	96	OR = 0.65(0.15–2.89)
History of anogenital injury
Yes	9.1	5.5	p = 0.38*
No	90.9	94.5	OR = 1.72(0.49–5.96)
Age at sexual debut
≥ 18 years	84.8	76.2	p = 0.19*
< 18 years	15.2	23.8	OR = 0 .29(0.04–2.13)
Sexual orientation
Heterosexual	97	99.3	p = 0.17*
Other	3	0.7	OR = 0.24(0.03–2.18)
Number of lifetime male partners
1 or 0	97	99.6	p = 0.38*
> 1	3	0.4	OR = 8.5(0.75–96.24)
Number of lifetime female partners
1 or 0	45.5	65.4	p = 0.02
> 1	54.5	34.6	OR = 2.27(1.12–4.60)
Number of last year's female partners
1 or 0	93.9	89.9	p = 0.45*
> 1	6.1	10.1	OR = 2.27(1.12–4.60)
Sex with sex workers
Yes	9.1	8.4	p = 0.89*
No	90.9	91.6	OR = 1.09(0.32–3.70)
Sex with foreigners
Yes	6.1	1.3	p = 0.03*
No	93.9	98.7	OR = 4.96(0.99–24.91)
Total	100	100

Table − 1 – Characteristics of study participant stratified by HPV & associated factors *Exact significance** Married -(legally or customarily) and married but separated/divorced/widowed

The logistic regression analysis was carried out to identify the factors that independently determine the risk of HPV infection. The lifetime number of female sexual partners (p = 0.02) and marital status (p = 0.04) as independent variables showed statistical significance. The lifetime number of female sex partners was a predictor of HPV infection among sexually active men recording an adjusted OR of 2.4 (95% CI:1.1–4.9). The men who had more than one female sexual partner in their lifetime have a 2.4 times higher risk of getting HPV infection after controlling for all other factors in the model compared to men who had 1 or 0 female sexual partner/s. The unmarried sexually active participants have adjusted OR of 3.5(95%CI:1.01–12.1) or 3.5 times higher risk compared to married sexually active men after controlling for all other factors in the model.

Table − 2 Correlates of HPV prevalence in normal men after multivariate analysis

Characteristic	β	S.E.	p value	Adjusted OR (Exp β)	95% CI, for adjusted OR (Exp β)
Characteristic	β	S.E.	p value	Adjusted OR (Exp β)	Lower	Upper
Lifetime female sex partners	0.87	0.38	0.02	2.4	1.1	4.9
Sexual orientation	1.9	1.16	0.1	0.2	0.02	1.5
Marital Status	1.26	0.63	0.04	3.5	1.04	12.1
Sex with foreigners	1.19	0.86	0.17	3.3	0.6	17.8
Sexual debut	1.22	1.04	0.24	0.3	0.04	2.3
Constant	2.57	2.88	0.37	0.08

The present study is the first community based study to describe the HPV prevalence among men in Sri Lanka. The non-response rate was assumed to be 10% and did not exceed this limit during the data collection. The basic sociodemographic characteristics of non-responders were similar to those of responders, serving to minimize selection bias. The urban-to-rural population, male-to-female sex ratio and distribution of age categories among study subjects were closely comparable to the overall country enabling generalizability(12). The use of PCR with the consensus primer GP5+/GP6+, which is the most employed sensitive method for HPV detection allows the comparison of findings of the present study with those of other countries(13).

The mean age of the study participants was 39.7 years (± SD = 12.5). The mean age of sexual debut was 22.3 years (± SD = 5), 76.3% was legally or customarily married; 99.1% was heterosexual and 0.9% was bisexual. Other factors for HPV acquisition and persistence such as; anogenital warts (3.1%), phimosis (5.2%), and history of anogenital injury (5.7%) were identified in low proportions among clinically healthy people. However, having more than one lifetime sexual female partner (35.8%) was reported as a considerable proportion, with the majority practicing penovaginal sex (66.5%). It is noteworthy that 53.2% of participants had never used condoms during sexual practices. The overall HPV prevalence among clinically normal men in the community was 5.7% (95% CI: 3.96–7.91), with a high-risk HPV prevalence of genotype HPV16 and HPV 59, 1.7% (95% CI:0.8–3.1). Significant factors for HPV prevalence among clinically normal men after adjusting for confounding factors were, having multiple female sex partners (adjusted OR of 2.4 ,95% CI: 1.1–4.9) compared to those with a single or no female sex partner and engaged in sexual relationships being unmarried (adjusted OR of 3.5 ,95% CI: 1.04–12.1) compared to those who are married.

This community prevalence rate was relatively high compared to the figure of 1.3% (95% CI:0.01,7.2) reported in Japan in 2003 (14). There were a limited number of studies conducted in the Asian region with relatively small sample sizes that examined penile HPV prevalence among male partners of women participating in cervical cancer research with findings varying from 26.7% in India (2006) (15),4.7% in the Philippines (2004) and 17.3% in Thailand (2002)(16). The overall prevalence of any HPV infection estimated in a community-based study in China was 10.5% (17), and a cohort study in China in 2015 recorded it as 16.9%(n = 2228) (5). A cross-sectional study in Malaysia (2014–2016) among 503 males aged 18–60 found a genital HPV prevalence of 29.6%(18). The high prevalence may be attributed to increased high-risk sexual behaviours compared to Sri Lanka. Differences in results could also be due to the Malaysian study's use of non-specific site specimens and convenient sampling of clinic attendees' companions, compared to the present study's use of penile samples and community cluster sampling, which reduce selection bias. The HPV In Men(HIM), study combined genital samples of 1,160 clinically normal men from Brazil, Mexico, and the United States revealing an estimated overall HPV prevalence among heterosexual men of 65.2%, with individual countries Brazil, United States Mexico revealing 72.3%, 61.3% and 61.9% respectively (19). Additionally, a systematic review conducted among Brazilian men revealed that the prevalence was 36.21% (95% CI 23.40, 51.33) in the penile specimen (20). A study among sexually active adolescents and young adults estimated male HPV prevalence for any HPV type was 29.2%(21). Remarkably, the community prevalence rates observed in Western countries significantly surpassed those recorded in the current community-based prevalence study, in the Sri Lanka.

In the present community prevalence study, the most frequent HR HPV types detected were 59,16,45 and 31 LR HPV types were 81,90,7,42,6,62,73, 89. A study done in Sri Lanka in 2008 among females revealed common HR HPV genotypes 16 and 18 was 1.2% (95% CI:1.15–1.2) (Gamage, 2017). A systematic review and meta-analysis of studies published between 1995 and 2022 included population-based surveys in men aged 15 years or older. It identified 65 studies (n = 44769 men) from 35 countries and reported a global pooled prevalence of 21% (95%CI:18.0,24.0) for HR-HPV. HPV-16 was the most prevalent HPV genotype with a prevalence of 5%, (95% CI, 4.0-7.2) followed by the HPV-6 genotype being 4% (95% CI, 3.3–5.1). In this present study, it was 30.3% (10/33) of HPV types were HR types in a community-based study and the most prevalent type was HPV 59 followed by HPV 16,31 and 45. The high prevalence of HPV genotype 59 highlights the need to include this strain in future vaccine development, as recognized by Mexico to combat HPV-related cancers. (22).

A statistically significant difference in prevalence rates was not observed among the age of age categories, ethnicity groups or religious groups in this study. It has been reported in global literature too that anogenital HPV prevalence does not vary across age groups (p = 0.952) and different races (p = 0.820) (18). In addition a significant difference in prevalence rates was not observed with current employment status, income of the respondent and level of education in the present study. However, this is in contrast to the high prevalence that was observed (77% in the penile shaft and 66% in the coronal sulcus) in Chille (23),and 8.7%n(n = 313) as reported in Korea among university students. However, in none of these studies, a significant association of the prevalence has been reported with the level of education.

Statistically significant associations of the prevalence were not observed with a history of phimosis, circumcision and anogenital injury among present study partners. These findings are on par with that of the HIM (HPV in Men) study the only prospective multi-center international cohort study with a large sample size, that reported phimosis and circumcision as not having significant associations with HPV infection. However, in contrast to the findings of the present community study, the HIM study found a significant association between a history of genital warts and HPV infection (19). Moderate alcohol consumption has been reported to be significantly associated with recurrence (OR, 1.59; 95% CI:1.01–2.53) compared with mild alcohol consumption in HPV-men-follow-up study (24). In the present study, tobacco (p = 0.05) and alcohol (p = 0.024) consumption were significantly associated with HPV infection in bivariable analysis, however, these associations were not observed following adjusting for confounders in logistic regression analysis as in Malaysian community-based study (25). In this present study, there was no significant difference observed based on sexual orientation, Notably, more than half (53.2%) of the participants, engage in sexual activities without using condoms implying the requirement of proper sex education and promoting safer sexual practices.

The Giuliano's study found that older age at sexual initiation is associated with a significantly reduced risk of HPV infection, indicating that early initiation may increase vulnerability (19).The mean age of sexual debut was 22.3 (SD ± 5) years with no statistically significant difference in HPV prevalence rates among the age of sexual debut < 18 years and > 18 years in this study, compared to 18.6 (SD ± 1.8) years in previous Sri Lankan surveys, (26). However results of this study revealed that having sex being unmarried carries a higher risk of getting HPV infection (adjusted OR of 3.5 ,95% CI: 1.04–12.1) compared to marital sex. Compatibly having a stable partner was linked to lower risks for HPV infection, with OR ranging from 0.55 to 0.58 reported in previous studies(27).In this study, 35.8% of community participants reported having more than one female sexual partner during their lifetime. In literature numerous studies have reported a strong association between HPV and promiscuous sex. A significant association (p = 0.002, adjusted OR of 2.4 ,95% CI: 1.1–4.9) was observed between having > 1 female partner and HPV infection compared to having 1 or no female partners. Similarly, in multi-country study reported having more than 3 sexual partners(p = 0.05,OR-3.87) and study in United State, having > 5 vaginal sexual partner(p = 0.0108) were significantly associated with HPV infection(16)(28).Notably, having over 50 lifetime sexual partners verses 1 sexual partner increased the risk, with an OR of 2.3, highlighting the strong link between multiple sexual partners and elevated HPV infection risk studies across world(29).

However, sex-related questions were sensitive and may have responded negatively even though all measures have been taken to collect correct information. These unavoidable reasons may have contributed to possible misclassification bias. HPV can infect various anatomical sites, including the penis, anus, and throat. In the study, only penile samples were collected it would have been better if all possible anatomical sites were sampled to understand factors contributing to the acquisition and persistence of HPV infection.

High-risk sexual behaviours are significantly associated with HPV infection. Promoting safe sex practices, along with ongoing detection and monitoring of vaccine-preventable HPV genotypes among males is vital for decision-making for preventive strategies. Further future policies should require an economic evaluation based on this prevalence before adopting a gender-neutral approach with a single- or two-dose schedule, in line with the new WHO recommendations

Ethics approval and consent to participate

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee in the Post Graduate Institute of Medicine Colombo22.07.2022 to 22.07.2023 and the research ethics review committee of WHO regional office for South-East Asia (‎SEARO-ERC)) 23.08.2022. Informed written consent was secured before the study. All measures were taken to minimize risk and maximize benefits. Participation was voluntary, with the option to withdraw at any time without penalty or loss of medical care. Informed written consent was obtained from all subjects involved in the study to publish this paper.

Consent for publication-Not applicable

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests

Funding

The research leading to these results received funding from the World Health Organization, via the Epidemiology Unit of the Ministry of Health

Authors' Contributions:

The principal author analyzed and interpreted the patient data on HPV prevalence among males and associated factors and contributed to drafting the manuscript. The two other authors served as supervisors, overseeing all stages of the research and contributing to each step of the process. All authors read and approved the final manuscript.

Acknowledgements

Dr.P.K.B.Mahesh, Dr.Samitha Ginige Dr.Manjula Kariyawasam

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Penile HPV prevalence and associated factors among 20–70-year-old men in Sri Lanka: A Study in a Lower& Middle-Income Country

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