Human papillomavirus carriage in the semen of men consulting for infertility: prevalence and correlations with sperm characteristics.


Journal

Asian journal of andrology
ISSN: 1745-7262
Titre abrégé: Asian J Androl
Pays: China
ID NLM: 100942132

Informations de publication

Date de publication:
22 Oct 2024
Historique:
received: 09 01 2024
accepted: 17 07 2024
medline: 22 10 2024
pubmed: 22 10 2024
entrez: 22 10 2024
Statut: aheadofprint

Résumé

We aim to study the semen carriage of human papillomavirus (HPV) and evaluate its association with patient characteristics. We conduct a single-center cohort study at Amiens University Hospital Center (Amiens, France). From May 1 to October 31, 2021, 461 men consulting for infertility and with semen analysis data were included. Each participant gave his written informed consent for the use of laboratory, demographic, clinical, and lifestyle data. A proportion of the semen samples were sent to a virology laboratory for HPV screening in a polymerase chain reaction (PCR) assay. In univariate and multivariate analyses with a logistic regression model, HPV+ and HPV- groups were compared with regard to semen characteristics (including the DNA fragmentation index and the sperm decondensation index) and demographic, clinical, and lifestyle variables. Semen HPV carriage was detected in 22.3% of the patients. High-oncogenic-risk HPV genotypes were predominant (57.6%). Multivariate analysis showed that HPV carriage was significantly associated with the presence of at least one abnormal spermogram dinging (according to the 6th World Health Organization criteria), with an adjusted odds ratio (OR) of 4.10 (95% confidence interval [CI]: 2.32-7.25, P < 0.001). A statistically significant association was also found for the type of infertility (OR: 1.61, 95% CI: 1.00-2.57, P = 0.05), the presence of varicocele (OR: 3.99, 95% CI: 1.48-10.71, P = 0.01), and a history of cryptorchidism, testicular ectopia, or monorchidism (OR: 3.54, 95% CI: 1.07-11.66, P = 0.04). Infection with a single HPV genotype or multiple HPV genotypes was significantly associated with at least one abnormal spermogram finding for all HPV oncogenic risk groups (OR: 3.93, 95% CI: 2.08-7.41, P < 0.001; and OR: 4.11, 95% CI: 1.58-10.68, P = 0.01, respectively). The association between sperm HPV carriage and the risk of infertility was statistically significant in a multivariate analysis (OR: 5.63, 95% CI: 3.16-10.01, P < 0.001) and after adjustment for the propensity score (OR: 6.10, 95% CI: 3.33-11.21, P < 0.001). Our results suggest that semen HPV carriage has an impact on male fertility. Sperm screening for HPV might be a useful addition to the work-up for male infertility.

Identifiants

pubmed: 39435846
doi: 10.4103/aja202458
pii: 00129336-990000000-00259
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 Copyright: ©The Author(s)(2024).

Références

Trottier H, Franco EL The epidemiology of genital human papillomavirus infection. Vaccine 2006; 24 Suppl 1 1–15.
De Sanjosé S, Brotons M, Pavón MA The natural history of human papillomavirus infection. Best Pract Res Clin Obstet Gynaecol 2018; 47: 2–13.
Repp KK, Nielson CM, Fu R, Schafer S, Lazcano-Ponce E, et al. Male human papillomavirus prevalence and association with condom use in Brazil, Mexico, and the United States. J Infect Dis 2012; 205: 1287–93.
Thierry P, Lasserre A, Rossignol L, Kernéis S, Blaizeau F, et al. Human papillomavirus vaccination in general practice in France, three years after the implementation of a targeted vaccine recommendation based on age and sexual history. Hum Vaccin Immunother 2015; 12: 528–33.
Moreno-Sepulveda J, Rajmil O Seminal human papillomavirus infection and reproduction: a systematic review and meta-analysis. Andrology 2021; 9: 478–502.
Schillaci R, Capra G, Bellavia C, Ruvolo G, Scazzone C, et al. Detection of oncogenic human papillomavirus genotypes on spermatozoa from male partners of infertile couples. Fertil Steril 2013; 100: 1236–40.
Depuydt CE, Donders GG, Verstraete L, Broeck DV, Beert JF, et al. Infectious human papillomavirus virions in semen reduce clinical pregnancy rates in women undergoing intrauterine insemination. Fertil Steril 2019; 111: 1135–44.
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen 6th ed. Geneva: World Health Organization; 2021.
Estrade C, Sahli R Comparison of seegene anyplex II HPV28 with the PGMY-CHUV assay for human papillomavirus genotyping. J Clin Microbiol 2014; 52: 607–12.
Dunne EF, Nielson CM, Stone KM, Markowitz LE, Giuliano AR Prevalence of HPV infection among men: a systematic review of the literature. J Infect Dis 2006; 194: 1044–57.
Laprise C, Trottier H, Monnier P, Coutlée F, Mayrand MH Prevalence of human papillomaviruses in semen: a systematic review and meta-analysis. Hum Reprod 2014; 29: 640–51.
Foresta C, Noventa M, De Toni L, Gizzo S, Garolla A HPV-DNA sperm infection and infertility: from a systematic literature review to a possible clinical management proposal. Andrology 2015; 3: 163–73.
Damke E, Kurscheidt FA, Balani VA, Takeda KI, Irie MM, et al. Male partners of infertile couples with seminal infections of human papillomavirus have impaired fertility parameters. Biomed Res Int 2017 2017 e4684629.
Lyu Z, Feng X, Li N, Zhao W, Wei L, et al. Human papillomavirus in semen and the risk for male infertility: a systematic review and meta-analysis. BMC Infect Dis 2017; 17: 714.
Garolla A, De Toni L, Bottacin A, Valente U, De Rocco Ponce M, et al. Human papillomavirus prophylactic vaccination improves reproductive outcome in infertile patients with HPV semen infection: a retrospective study. Sci Rep 2018; 8: 912.
Cao X, Wei R, Zhang X, Zhou J, Lou J, et al. Impact of human papillomavirus infection in semen on sperm progressive motility in infertile men: a systematic review and meta-analysis. Reprod Biol Endocrinol 2020; 18: 38.
Tanaka H, Karube A, Kodama H, Fukuda J, Tanaka T Mass screening for human papillomavirus type 16 infection in infertile couples. J Reprod Med 2000; 45: 907–11.
Fedder J, Ørnskov D, Engvad B, Kristensen TK, Lomholt M, et al. Seminal human papillomavirus originates from the body surface and is not a frequent aetiological factor in azoospermia. Andrologia 2019; 51: e13202.
Kim SJ, Paik DJ, Lee JS, Lee HS, Seo JT, et al. Effects of infections with five sexually transmitted pathogens on sperm quality. Clin Exp Reprod Med 2017; 44: 207–13.
Luttmer R, Dijkstra MG, Snijders PJ, Hompes PG, Pronk DT, et al. Presence of human papillomavirus in semen in relation to semen quality. Hum Reprod 2016; 31: 280–6.
Perino A, Giovannelli L, Schillaci R, Ruvolo G, Fiorentino FP, et al. Human papillomavirus infection in couples undergoing in vitro fertilization procedures: impact on reproductive outcomes. Fertil Steril 2011; 95: 1845–8.
Yang Y, Jia CW, Ma YM, Zhou LY, Wang SY Correlation between HPV sperm infection and male infertility. Asian J Androl 2013; 15: 529–32.
Golob B, Poljak M, Verdenik I, Kolbezen Simoniti M, Vrtačnik Bokal E, et al. High HPV infection prevalence in men from infertile couples and lack of relationship between seminal HPV infection and sperm quality. Biomed Res Int 2014 2014 e956901.
Foresta C, Garolla A, Parisi S, Ghezzi M, Bertoldo A, et al. HPV prophylactic vaccination in males improves the clearance of semen infection. EBioMedicine 2015; 2: 1487–93.
Moghimi M, Zabihi-Mahmoodabadi S, Kheirkhah-Vakilabad A, Kargar Z Significant correlation between high-risk HPV DNA in semen and impairment of sperm quality in infertile men. Int J Fertil Steril 2019; 12: 306–9.
Rossi T, Grandoni F, Mazzilli F, Quattrucci S, Antonelli M, et al. High frequency of (TG)mTn variant tracts in the cystic fibrosis transmembrane conductance regulator gene in men with high semen viscosity. Fertil Steril 2004; 82: 1316–22.
Elia J, Delfino M, Imbrogno N, Capogreco F, Lucarelli M, et al. Human semen hyperviscosity: prevalence, pathogenesis and therapeutic aspects. Asian J Androl 2009; 11: 609–15.
Du Plessis SS, Gokul S, Agarwal A Semen hyperviscosity: causes, consequences, and cures. Front Biosci 2013; 5: 224–31.
Xiong YQ, Chen YX, Cheng MJ, He WQ, Chen Q The risk of human papillomavirus infection for male fertility abnormality: a meta-analysis. Asian J Androl 2018; 20: 493–7.
Muscianisi F, De Toni L, Giorato G, Carosso A, Foresta C, et al. Is HPV the novel target in male idiopathic infertility? A systematic review of the literature. Front Endocrinol 2021; 12: e643539.
Wang RY, Li YJ, Lee WC, Wu HH, Lin CY, et al. The association between polyomavirus BK strains and BKV viruria in liver transplant recipients. Sci Rep 2016; 6: e28491.
Foresta C, Garolla A, Zuccarello D, Pizzol D, Moretti A, et al. Human papillomavirus found in sperm head of young adult males affects the progressive motility. Fertil Steril 2010; 93: 802–6.
Foresta C, Ferlin A, Bertoldo A, Patassini C, Zuccarello D, et al. Human papilloma virus in the sperm cryobank: an emerging problem?. Int J Androl 2011; 34: 242–6.
Boeri L, Capogrosso P, Ventimiglia E, Pederzoli F, Cazzaniga W, et al. High-risk human papillomavirus in semen is associated with poor sperm progressive motility and a high sperm DNA fragmentation index in infertile men. Hum Reprod 2019; 34: 209–17.
Foresta C, Patassini C, Bertoldo A, Menegazzo M, Francavilla F, et al. Mechanism of human papillomavirus binding to human spermatozoa and fertilizing ability of infected spermatozoa. PLoS One 2011; 6: e15036.
Gunderson S, Eskew AM, Stoutenburg D, Riley JK, Stout MJ, et al. Association of the human semen DNA virome with successful in vitro fertilization. F S Sci 2022; 3: 2–9.
Van Doornum GJ, Prins M, Juffermans LH, Hooykaas C, van den Hoek JA, et al. Regional distribution and incidence of human papillomavirus infections among heterosexual men and women with multiple sexual partners: a prospective study. Genitourin Med 1994; 70: 240–6.

Auteurs

Armin Priam (A)

Urology Department, Amiens University Hospital Center, Amiens 80000, France.
Reproductive Medicine Department, Amiens University Hospital Center, Amiens 80000, France.

Antoine Le Bozec (AL)

Pharmacy Department, Kremlin Bicêtre Hospital, Paris-Saclay University, Le Kremlin-Bicêtre 94270, France.

Vasco Dias Meireles (VD)

AGIR Research Unit 4294, Picardie-Jules Verne University, Amiens 80000, France.
Virology Department, Amiens University Hospital Center, Amiens 80000, France.

Fabien Saint (F)

Urology Department, Amiens University Hospital Center, Amiens 80000, France.
EPROAD Research Unit 4669, Picardie-Jules Verne University, Amiens 80000, France.

Rosalie Cabry (R)

Reproductive Medicine Department, Amiens University Hospital Center, Amiens 80000, France.
PERITOX Research Unit UMR-I-01, Picardie-Jules Verne University, Amiens 80000, France.

Moncef Benkhalifa (M)

Reproductive Medicine Department, Amiens University Hospital Center, Amiens 80000, France.
PERITOX Research Unit UMR-I-01, Picardie-Jules Verne University, Amiens 80000, France.

Baptiste Demey (B)

AGIR Research Unit 4294, Picardie-Jules Verne University, Amiens 80000, France.
Virology Department, Amiens University Hospital Center, Amiens 80000, France.

Dorian Bosquet (D)

Reproductive Medicine Department, Amiens University Hospital Center, Amiens 80000, France.
PERITOX Research Unit UMR-I-01, Picardie-Jules Verne University, Amiens 80000, France.

Classifications MeSH