Male infertility: A public health issue caused by sexually transmitted pathogens

Nature Reviews Urology

Volumn 11, Issue 12, 2014, Pages 672-687

  Gimenes, Fabrícia ^a   Souza, Raquel P ^a   Bento, Jaqueline C ^c   Teixeira, Jorge J V ^b   Maria Engler, Silvya S ^a   Bonini, Marcelo G ^d   Consolaro, Marcia E L ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

^b Sao Camilo Clinical Analysis Laboratory   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL INFECTION; CHLAMYDIA TRACHOMATIS; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; MALE INFERTILITY; MYCOPLASMA; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTOZOAL INFECTION; REVIEW; SEXUALLY TRANSMITTED DISEASE; SPERM; TREPONEMA PALLIDUM; TRICHOMONAS VAGINALIS; UREAPLASMA; VIRUS INFECTION; WART VIRUS; COMPLICATION; CYTOMEGALOVIRUS; HEPACIVIRUS; MALE; MICROBIOLOGY; PAPILLOMAVIRIDAE; PARASITOLOGY; SEMEN ANALYSIS; SIMPLEXVIRUS; TRANSMISSION; VIROLOGY;

CHLAMYDIA TRACHOMATIS; CYTOMEGALOVIRUS; HEPACIVIRUS; HEPATITIS B VIRUS; HIV; HUMANS; INFERTILITY, MALE; MALE; MYCOPLASMA; NEISSERIA GONORRHOEAE; PAPILLOMAVIRIDAE; SEMEN; SEMEN ANALYSIS; SEXUALLY TRANSMITTED DISEASES; SIMPLEXVIRUS; TREPONEMA PALLIDUM; TRICHOMONAS VAGINALIS; UREAPLASMA;

EID: 84927572539     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2014.285     Document Type: Review

References (296)

1. Ochsendorf, F. R. Sexually transmitted infections: impact on male fertility. Andrologia 40, 72-75 (2008
2. Muvunyi, C. M. et al. Decreased susceptibility to commonly used antimicrobial agents in bacterial pathogens isolated from urinary tract infections in Rwanda: need for new antimicrobial guidelines. Am. J. Trop. Med. Hyg. 84, 923-928 (2011
3. Garolla, A. et al. Sperm viral infection and male infertility: focus on HBV, HCV, HIV, HPV, HSV, HCMV, and AAV. J. Reprod. Immunol. 100, 20-29 (2013
4. Rowe, P. J., Comhaire, F. H., Hargreave, T. B. &Mahmoud, A. M. A. WHO manual for the standardized investigation, diagnosis and management of the infertile male (Cambridge University Press, 2000
5. Brookings, C., Goldmeier, D. &Sadeghi-Nejad, H. Sexually transmitted infections and sexual function in relation to male fertility. Korean J. Urol. 54, 149-156 (2013
6. Monavari, S. H. et al. Asymptomatic seminal infection of herpes simplex virus: impact on male infertility. J. Biomed. Res. 27, 56-61 (2013
7. Muciaccia, B. et al. HIV-1 viral DNA is present in ejaculated abnormal spermatozoa of seropositive subjects. Hum. Reprod. 22, 2868-2878 (2007
8. Al-Daghistani, H. I., Hamad, A. W., Abdel-Dayem, M., Al-Swaifi, M. &Abu Zaid, M. Evaluation of serum testosterone, progesterone, seminal antisperm antibody, and fructose levels among Jordanian males with a history of infertility. Biochem. Res. Int. 2010, 409640 (2010
9. Lee, J. S. et al. Concordance of Ureaplasma urealyticum and Mycoplasma hominis in infertile couples: impact on semen parameters. Urology 81, 1219-1224 (2013
10. Pekler, V. A. et al. Use of versant TMA and bDNA 3.0 assays to detect and quantify hepatitis C virus in semen. J. Clin. Lab. Anal. 17, 264-270 (2003
11. Kapranos, N., Petrakou, E., Anastasiadou, C. &Kotronias, D. Detection of herpes simplex virus, cytomegalovirus, and Epstein-Barr virus in the semen of men attending an infertility clinic. Fertil. Steril. 79 (Suppl. 3), 1566-1570 (2003
12. Hamdad-Daoudi, F., Petit, J. &Eb, F. Assessment of Chlamydia trachomatis infection in asymptomatic male partners of infertile couples. J. Med. Microbiol. 53, 985-990 (2004
13. Bayasgalan, G., Naranbat, D., Radnaabazar, J., Lhagvasuren, T. &Rowe, P. J. Male infertility: risk factors in Mongolian men. Asian J. Androl. 6, 305-311 (2004
14. Bezold, G. et al. Prevalence of sexually transmissible pathogens in semen from asymptomatic male infertility patients with and without leukocytospermia. Fertil. Steril. 87, 1087-1097 (2007
15. Rusz, A. et al. Influence of urogenital infections and inflammation on semen quality and male fertility. World J. Urol. 30, 23-30 (2012
16. Moretti, E., Federico, M. G., Giannerini, V. &Collodel, G. Sperm ultrastructure and meiotic segregation in a group of patients with chronic hepatitis B and C. Andrologia 40, 286-291 (2008
17. Grunewald, S. et al. Caspase activation in human spermatozoa in response to physiological and pathological stimuli. Fertil. Steril. 83 (Suppl. 1), 1106-1112 (2005
18. Koppers, A. J., De Iuliis, G. N., Finnie, J. M., McLaughlin, E. A. &Aitken, R. J. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab. 93, 3199-3207 (2008
19. Ricci, G. et al. Apoptosis in human sperm: its correlation with semen quality and the presence of leukocytes. Hum. Reprod. 17, 2665-2672 (2002
20. Moustafa, M. H. et al. Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum. Reprod. 19, 129-138 (2004
21. Ochsendorf, F. R. Infections in the male genital tract and reactive oxygen species. Hum. Reprod. Update 5, 399-420 (1999
22. Flesch, F. M. &Gadella, B. M. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim. Biophys. Acta 1469, 197-235 (2000
23. Souza, R. P. et al. Simultaneous detection of seven sexually transmitted agents in human immunodeficiency virus-infected Brazilian women by multiplex polymerase chain reaction. Am. J. Trop. Med. Hyg. 89, 1199-1202 (2013
24. Rybar, R. et al. The effect of bacterial contamination of semen on sperm chromatin integrity and standard semen parameters in men from infertile couples. Andrologia 44 (Suppl. 1), 410-418 (2012
25. Villegas, J., Schulz, M., Soto, L. &Sanchez, R. Bacteria induce expression of apoptosis in human spermatozoa. Apoptosis 10, 105-110 (2005
26. Isaiah, I. N., Nche, B. T., Nwagu, I. G. &Nnanna, I. I. Current studies on bacterospermia the leading cause of male infertility: a protege and potential threat towards mans extinction. N. Am. J. Med. Sci. 3, 562-564 (2011
27. Cunningham, K. A. &Beagley, K. W. Male genital tract chlamydial infection: implications for pathology and infertility. Biol. Reprod. 79, 180-189 (2008
28. Mylonas, I. Female genital Chlamydia trachomatis infection: where are we heading? Arch. Gynecol. Obstet. 285, 1271-1285 (2012
29. Senior, K. Chlamydia: a much underestimated STI. Lancet Infect. Dis. 12, 517-518 (2012
30. Mackern-Oberti, J. P. et al. Chlamydia trachomatis infection of the male genital tract: an update. J. Reprod. Immunol. 100, 37-53 (2013
31. LaMontagne, D. S., Fenton, K. A., Randall, S., Anderson, S. &Carter, P. Establishing the National Chlamydia Screening Programme in England: results from the first full year of screening. Sex. Transm. Infect. 80, 335-341 (2004
32. Gdoura, R. et al. Assessment of Chlamydia trachomatis, Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis, and Mycoplasma genitalium in semen and first void urine specimens of asymptomatic male partners of infertile couples. J. Androl. 29, 198-206 (2008
33. Abusarah, E. A., Awwad, Z. M., Charvalos, E. &Shehabi, A. A. Molecular detection of potential sexually transmitted pathogens in semen and urine specimens of infertile and fertile males. Diagn. Microbiol. Infect. Dis. 77, 283-286 (2013
34. Nadala, E. C. et al. Performance evaluation of a new rapid urine test for chlamydia in men: prospective cohort study. BMJ 339, b2655 (2009
35. Kalwij, S., French, S., Mugezi, R. &Baraitser, P. Using educational outreach and a financial incentive to increase general practices' contribution to chlamydia screening in South-East London 2003-2011. BMC Public Health 12, 802 (2012
36. Ibrahim, A. A., Refeidi, A. &El Mekki, A. A. Etiology and clinical features of acute epididymo-orchitis. Ann. Saudi Med. 16, 171-174 (1996
37. Dale, A. W., Wilson, J. D., Forster, G. E., Daniels, D. &Brook, M. G. Management of epididymo-orchitis in Genitourinary Medicine clinics in the United Kingdom's North Thames region 2000. Int. J. STD AIDS 12, 342-345 (2001
38. Furuya, R. et al. Is seminal vesiculitis a discrete disease entity? Clinical and microbiological study of seminal vesiculitis in patients with acute epididymitis. J. Urol. 171, 1550-1553 (2004
39. Eley, A., Pacey, A. A., Galdiero, M., Galdiero, M. &Galdiero, F. Can Chlamydia trachomatis directly damage your sperm? Lancet Infect. Dis. 5, 53-57 (2005
40. Trojian, T. H., Lishnak, T. S. &Heiman, D. Epididymitis and orchitis: an overview. Am. Fam. Physician 79, 583-587 (2009
41. Mackern Oberti, J. P. et al. Chemokine response induced by Chlamydia trachomatis in prostate derived CD45+ and CD45-cells. Reproduction 142, 427-437 (2011
42. Motrich, R. D., Sanchez, L., Maccioni, M., Mackern-Oberti, J. P. &Rivero, V. E. Male rat genital tract infection with Chlamydia muridarum has no significant consequence on male fertility. J. Urol. 187, 1911-1917 (2012
43. Pate, M. S. et al. Urethral cytokine and immune responses in Chlamydia trachomatis-infected males. Infect. Immun. 69, 7178-7181 (2001
44. Al-Mously, N. &Eley, A. Interaction of Chlamydia trachomatis serovar E with male genital tract epithelium results in secretion of proinflammatory cytokines. J. Med. Microbiol. 56, 1025-1032 (2007
45. Geisler, W. M. Duration of untreated, uncomplicated Chlamydia trachomatis genital infection and factors associated with chlamydia resolution: a review of human studies. J. Infect. Dis. 201 (Suppl. 2), S104-S113 (2010
46. Taylor, B. D. &Haggerty, C. L. Management of Chlamydia trachomatis genital tract infection: screening and treatment challenges. Infect. Drug Resist. 4, 19-29 (2011
47. Mackern-Oberti, J. P. et al. Innate immunity in the male genital tract: Chlamydia trachomatis induces keratinocyte-derived chemokine production in prostate, seminal vesicle and epididymis/vas deferens primary cultures. J. Med. Microbiol. 60, 307-316 (2011
48. Karinen, L. et al. Association between Chlamydia trachomatis antibodies and subfertility in the Northern Finland Birth Cohort 1966 (NFBC 1966), at the age of 31 years. Epidemiol. Infect. 132, 977-984 (2004
49. Joki-Korpela, P. et al. The role of Chlamydia trachomatis infection in male infertility. Fertil. Steril. 91, 1448-1450 (2009
50. Mazzoli, S. et al. Chlamydia trachomatis infection is related to poor semen quality in young prostatitis patients. Eur. Urol. 57, 708-714 (2010
51. Pajovic, B., Radojevic, N., Vukovic, M. &Stjepcevic, A. Semen analysis before and after antibiotic treatment of asymptomatic Chlamydia-And Ureaplasma-related pyospermia. Andrologia 45, 266-271 (2013
52. Motrich, R. D., Cuffini, C., Oberti, J. P., Maccioni, M. &Rivero, V. E. Chlamydia trachomatis occurrence and its impact on sperm quality in chronic prostatitis patients. J. Infect. 53, 175-183 (2006
53. de Barbeyrac, B. et al. Chlamydia trachomatis in subfertile couples undergoing an in vitro fertilization program: a prospective study. Eur. J. Obstet. Gynecol. Reprod. Biol. 129, 46-53 (2006
54. Henkel, R. et al. Chronic pelvic pain syndrome/chronic prostatitis affect the acrosome reaction in human spermatozoa. World J. Urol. 24, 39-44 (2006
55. Villegas, H., Pinon, M., Shor, V. &Karchmer, S. Electron microscopy of Chlamydia trachomatis infection of the male genital tract. Arch. Androl. 27, 117-126 (1991
56. Erbengi, T. Ultrastructural observations on the entry of Chlamydia trachomatis into human spermatozoa. Hum. Reprod. 8, 416-421 (1993
57. Hosseinzadeh, S., Brewis, I. A., Eley, A. &Pacey, A. A. Co-incubation of human spermatozoa with Chlamydia trachomatis serovar E causes premature sperm death. Hum. Reprod. 16, 293-299 (2001
58. Satta, A. et al. Experimental Chlamydia trachomatis infection causes apoptosis in human sperm. Hum. Reprod. 21, 134-137 (2006
59. Hosseinzadeh, S., Pacey, A. A. &Eley, A. Chlamydia trachomatis-induced death of human spermatozoa is caused primarily by lipopolysaccharide. J. Med. Microbiol. 52, 193-200 (2003
60. Hosseinzadeh, S., Brewis, I. A., Pacey, A. A., Moore, H. D. &Eley, A. Coincubation of human spermatozoa with Chlamydia trachomatis in vitro causes increased tyrosine phosphorylation of sperm proteins. Infect. Immun. 68, 4872-4876 (2000
61. Idahl, A., Boman, J., Kumlin, U. &Olofsson, J. I. Demonstration of Chlamydia trachomatis IgG antibodies in the male partner of the infertile couple is correlated with a reduced likelihood of achieving pregnancy. Hum. Reprod. 19, 1121-1126 (2004
62. Veznik, Z., Pospisil, L., Svecova, D., Zajicova, A. &Unzeitig, V. Chlamydiae in the ejaculate: their influence on the quality and morphology of sperm. Acta Obstet. Gynecol. Scand. 83, 656-660 (2004
63. Al-Mously, N., Cross, N. A., Eley, A. &Pacey, A. A. Real-time polymerase chain reaction shows that density centrifugation does not always remove Chlamydia trachomatis from human semen. Fertil. Steril. 92, 1606-1615 (2009
64. La Vignera, S., Condorelli, R. A., Vicari, E., D'Agata, R. &Calogero, A. E. Sperm DNA damage in patients with chronic viral C hepatitis. Eur. J. Intern. Med. 23, e19-e24 (2012
65. Jungwirth, A., Straberger, A., Esterbauer, B., Fink, K. &Schmeller, N. Acrosome reaction in Chlamydia-positive and negative patients. Andrologia 35, 314-316 (2003
66. Gallegos-Avila, G. et al. Phagocytosis of spermatozoa and leucocytes by epithelial cells of the genital tract in infertile men infected with Chlamydia trachomatis and mycoplasmas. Histopathology 55, 232-234 (2009
67. Ouzounova-Raykova, V., Ouzounova, I. &Mitov, I. G. May Chlamydia trachomatis be an aetiological agent of chronic prostatic infection? Andrologia 42, 176-181 (2010
68. Segnini, A., Camejo, M. I. &Proverbio, F. Chlamydia trachomatis and sperm lipid peroxidation in infertile men. Asian J. Androl. 5, 47-49 (2003
69. Habermann, B. &Krause, W. Altered sperm function or sperm antibodies are not associated with chlamydial antibodies in infertile men with leucocytospermia. J. Eur. Acad. Dermatol. Venereol. 12, 25-29 (1999
70. Vigil, P., Morales, P., Tapia, A., Riquelme, R. &Salgado, A. M. Chlamydia trachomatis infection in male partners of infertile couples: incidence and sperm function. Andrologia 34, 155-161 (2002
71. Eggert-Kruse, W. et al. Prevalence of Chlamydia trachomatis in subfertile couples. Fertil. Steril. 80, 660-663 (2003
72. Korenromp, E. L. et al. What proportion of episodes of gonorrhoea and chlamydia becomes symptomatic? Int. J. STD AIDS 13, 91-101 (2002
73. World Health Organization. Prevalence and incidence of selected sexually transmitted infections, Chlamydia trachomatis, Neisseria gonorrhoeae, syphilis and Trichomonas vaginalis: methods and results used by WHO to generate 2005 estimates [online], http://whqlibdoc.who.int/publications/2011/9789241502450-eng.pdf (2011
74. Rodriguez-Tirado, C. et al. Neisseria gonorrhoeae induced disruption of cell junction complexes in epithelial cells of the human genital tract. Microbes Infect. 14, 290-300 (2012
75. Parti, R. P., Horbay, M. A., Liao, M. &Dillon, J. A. Regulation of minD by oxyR in Neisseria gonorrhoeae. Res. Microbiol. 164, 406-415 (2013
76. Fang, L., Oliver, A., Jayaraman, G. C. &Wong, T. Trends in age disparities between younger and middle-Age adults among reported rates of chlamydia, gonorrhea, and infectious syphilis infections in Canada: findings from 1997 to 2007. Sex. Transm. Dis. 37, 18-25 (2010
77. Ehrhardt, A. A., Bolan, G. &Wasserheit, J. N. in Sexually transmitted diseases. 3rd edn Ch. 8 (eds Holmes, K. K. et al.) 117-127 (McGraw-Hill, 1999
78. Edwards, J. L. &Apicella, M. A. The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin. Microbiol. Rev. 17, 965-981 (2004
79. Mlisana, K. et al. Symptomatic vaginal discharge is a poor predictor of sexually transmitted infections and genital tract inflammation in high-risk women in South Africa. J. Infect. Dis. 206, 6-14 (2012
80. Kline, K. A., Sechman, E. V., Skaar, E. P. &Seifert, H. S. Recombination, repair and replication in the pathogenic Neisseriae: the 3 R's of molecular genetics of two human-specific bacterial pathogens. Mol. Microbiol. 50, 3-13 (2003
81. Pellati, D. et al. Genital tract infections and infertility. Eur. J. Obstet. Gynecol. Reprod. Biol. 140, 3-11 (2008
82. Radek, S. et al. Bacterial infection as a cause of infertility in humans [Czech]. Epidemiol. Mikrobiol. Imunol. 62, 26-32 (2013
83. Dohle, G. R. Inflammatory-Associated obstructions of the male reproductive tract. Andrologia 35, 321-324 (2003
84. Osegbe, D. N. Testicular function after unilateral bacterial epididymo-orchitis. Eur. Urol. 19, 204-208 (1991
85. Ludwig, M. Diagnosis and therapy of acute prostatitis, epididymitis and orchitis. Andrologia 40, 76-80 (2008
86. Akre, O. et al. Human fertility does not decline: evidence from Sweden. Fertil. Steril. 71, 1066-1069 (1999
87. Fox, K. K. et al. Longitudinal evaluation of serovar-specific immunity to Neisseria gonorrhoeae. Am. J. Epidemiol. 149, 353-358 (1999
88. Zhu, W. et al. Neisseria gonorrhoeae suppresses dendritic cell-induced, antigen-dependent CD4 T cell proliferation. PLoS ONE 7, e41260 (2012
89. Danaher, R. J. et al. Genetic basis of Neisseria gonorrhoeae lipooligosaccharide antigenic variation. J. Bacteriol. 177, 7275-7279 (1995
90. Gantner, F. et al. CD40-dependent and-independent activation of human tonsil B cells by CpG oligodeoxynucleotides. Eur. J. Immunol. 33, 1576-1585 (2003
91. Gringhuis, S. I. et al. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26, 605-616 (2007
92. Ram, S. et al. Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 188, 671-680 (1998
93. Shafer, W. M. et al. Phase variable changes in genes lgtA and lgtC within the lgtABCDE operon of Neisseria gonorrhoeae can modulate gonococcal susceptibility to normal human serum. J. Endotoxin Res. 8, 47-58 (2002
94. van Vliet, S. J. et al. Variation of Neisseria gonorrhoeae lipooligosaccharide directs dendritic cell-induced T helper responses. PLoS Pathog. 5, e1000625 (2009
95. Liu, Y., Liu, W. &Russell, M. W. Suppression of host adaptive immune responses by Neisseria gonorrhoeae: role of interleukin 10 and type 1 regulatory T cells. Mucosal Immunol. 7, 165-176 (2014
96. Manhart, L. E., Broad, J. M. &Golden, M. R. Mycoplasma genitalium: should we treat and how? Clin. Infect. Dis. 53 (Suppl. 3), S129-S142 (2011
97. Deguchi, T. &Maeda, S. Mycoplasma genitalium: another important pathogen of nongonococcal urethritis. J. Urol. 167, 1210-1217 (2002
98. Maeda, S. et al. Detection of Mycoplasma genitalium, Mycoplasma hominis, Ureaplasma parvum (biovar 1) and Ureaplasma urealyticum (biovar 2) in patients with non-gonococcal urethritis using polymerase chain reaction-microtiter plate hybridization. Int. J. Urol. 11, 750-754 (2004
99. Soni, S. et al. The prevalence of urethral and rectal Mycoplasma genitalium and its associations in men who have sex with men attending a genitourinary medicine clinic. Sex. Transm. Infect. 86, 21-24 (2010
100. Andrade-Rocha, F. T. Ureaplasma urealyticum and Mycoplasma hominis in men attending for routine semen analysis. Prevalence, incidence by age and clinical settings, influence on sperm characteristics, relationship with the leukocyte count and clinical value. Urol. Int. 71, 377-381 (2003
101. Wang, Y., Sun, G., Pan, J. G. &Li, T. Correlation of Ureaplasma urealyticum and Chlamydia trachomatis infections with male sterility: a meta-Analysis of randomized control trials [Chinese]. Zhonghua Nan Ke Xue 12, 615-618 (2006
102. Al-Sweih, N. A., Al-Fadli, A. H., Omu, A. E. &Rotimi, V. O. Prevalence of Chlamydia trachomatis, Mycoplasma hominis, Mycoplasma genitalium, and Ureaplasma urealyticum infections and seminal quality in infertile and fertile men in Kuwait. J. Androl. 33, 1323-1329 (2012
103. Wikstrom, A. &Jensen, J. S. Mycoplasma genitalium: a common cause of persistent urethritis among men treated with doxycycline. Sex. Transm. Infect. 82, 276-279 (2006
104. Uuskula, A. &Kohl, P. K. Genital mycoplasmas, including Mycoplasma genitalium, as sexually transmitted agents. Int. J. STD AIDS 13, 79-85 (2002
105. Jensen, J. S. Mycoplasma genitalium: the aetiological agent of urethritis and other sexually transmitted diseases. J. Eur. Acad. Dermatol. Venereol. 18, 1-11 (2004
106. Krieger, J. N. &Riley, D. E. Prostatitis: what is the role of infection. Int. J. Antimicrob. Agents 19, 475-479 (2002
107. Svenstrup, H. F., Fedder, J., Abraham-Peskir, J., Birkelund, S. &Christiansen, G. Mycoplasma genitalium attaches to human spermatozoa. Hum. Reprod. 18, 2103-2109 (2003
108. Volgmann, T., Ohlinger, R. &Panzig, B. Ureaplasma urealyticum-harmless commensal or underestimated enemy of human reproduction? A review. Arch. Gynecol. Obstet. 273, 133-139 (2005
109. Zeighami, H., Peerayeh, S. N., Yazdi, R. S. &Sorouri, R. Prevalence of Ureaplasma urealyticum and Ureaplasma parvum in semen of infertile and healthy men. Int. J. STD AIDS 20, 387-390 (2009
110. Zinzendorf, N. Y. et al. Ureaplasma urealyticum or Mycoplasma hominis infections and semen quality of infertile men in Abidjan. J. Reprod. Contraception 19, 65-72 (2008
111. Povlsen, K., Jensen, J. S. &Lind, I. Detection of Ureaplasma urealyticum by PCR and biovar determination by liquid hybridization. J. Clin. Microbiol. 36, 3211-3216 (1998
112. Badalyan, R. R., Fanarjyan, S. V. &Aghajanyan, I. G. Chlamydial and ureaplasmal infections in patients with nonbacterial chronic prostatitis. Andrologia 35, 263-265 (2003
113. Salari, M. H. &Karimi, A. Prevalence of Ureaplasma urealyticum and Mycoplasma genitalium in men with non-gonococcal urethritis. East Mediterr. Health J. 9, 291-295 (2003
114. Pannekoek, Y. et al. Cytokine concentrations in seminal plasma from subfertile men are not indicative of the presence of Ureaplasma urealyticum or Mycoplasma hominis in the lower genital tract. J. Med. Microbiol. 49, 697-700 (2000
115. Shang, X. J. et al. Ureaplasma urealyticum infection and apoptosis of spermatogenic cells. Asian J. Androl. 1, 127-129 (1999
116. Bornman, M. S. et al. Microbial flora in semen of infertile African men at Garankuwa hospital. Andrologia 22, 118-121 (1990
117. Xu, C., Sun, G. F., Zhu, Y. F. &Wang, Y. F. The correlation of Ureaplasma urealyticum infection with infertility. Andrologia 29, 219-226 (1997
118. Reichart, M., Levi, H., Kahane, I. &Bartoov, B. Dual energy metabolism-dependent effect of Ureaplasma urealyticum infection on sperm activity. J. Androl. 22, 404-412 (2001
119. Reichart, M., Kahane, I. &Bartoov, B. In vivo and in vitro impairment of human and ram sperm nuclear chromatin integrity by sexually transmitted Ureaplasma urealyticum infection. Biol. Reprod. 63, 1041-1048 (2000
120. Montagut, J. M., Lepretre, S., Degoy, J. &Rousseau, M. Ureaplasma in semen and IVF. Hum. Reprod. 6, 727-729 (1991
121. Knox, C. L. et al. Ureaplasma parvum and Ureaplasma urealyticum are detected in semen after washing before assisted reproductive technology procedures. Fertil. Steril. 80, 921-929 (2003
122. Rodriguez-Cerdeira, C. &Silami-Lopes, V. G. Congenital syphilis in the 21st century. Actas Dermosifiliogr. 103, 679-693 (2012
123. Sadiq, S. T. et al. The effects of early syphilis on CD4 counts and HIV-1 RNA viral loads in blood and semen. Sex. Transm. Infect. 81, 380-385 (2005
124. Spielmann, N. et al. Time trends of syphilis and HSV-2 co-infection among men who have sex with men in the German HIV-1 seroconverter cohort from 1996-2007 Sex. Transm. Infect. 86, 331-336 (2010
125. Cox, D. L. et al. Surface immunolabeling and consensus computational framework to identify candidate rare outer membrane proteins of Treponema pallidum. Infect. Immun. 78, 5178-5194 (2010
126. Landau, E. Y. &Wainrach, B. Sperm-mediated host-derived DNA transfer as a new mechanism for immune system evasion of sexually transmitted genital tract pathogens. Med. Hypotheses 79, 408-412 (2012
127. Radolf, J. D., Norgard, M. V. &Schulz, W. W. Outer membrane ultrastructure explains the limited antigenicity of virulent Treponema pallidum. Proc. Natl Acad. Sci. USA 86, 2051-2055 (1989
128. Radolf, J. D., Caimano, M. J., Stevenson, B. &Hu, L. T. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat. Rev. Microbiol. 10, 87-99 (2012
129. Cheng, L. &Bostwick, D. G. (eds) Essentials of anatomic pathology (Springer, 2011
130. Dejucq, N. &Jegou, B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol. Mol. Biol. Rev. 65, 208-231 (2001
131. Lorusso, F. et al. Impact of chronic viral diseases on semen parameters. Andrologia 42, 121-126 (2010
132. Kalichman, S. C., Di Berto, G. &Eaton, L. Human immunodeficiency virus viral load in blood plasma and semen: review and implications of empirical findings. Sex. Transm. Dis. 35, 55-60 (2008
133. Englert, Y. et al. Medically assisted reproduction in the presence of chronic viral diseases. Hum. Reprod. Update 10, 149-162 (2004
134. Association of Biomedical Andrologists et al. UK guidelines for the medical and laboratory screening of sperm, egg and embryo donors (2008). Hum. Fertil. (Camb.) 11, 201-210 (2008
135. Akande, V., Turner, C., Horner, P., Horne, A. &Pacey, A. Impact of Chlamydia trachomatis in the reproductive setting: British Fertility Society Guidelines for practice. Hum. Fertil. (Camb.) 13, 115-125 (2010
136. Wingfield, M. &Cottell, E. Viral screening of couples undergoing partner donation in assisted reproduction with regard to EU Directives 2004/23/EC, 2006/17/EC and 2006/86/EC: what is the evidence for repeated screening? Hum. Reprod. 25, 3058-3065 (2010
137. Colon-Lopez, V., Ortiz, A. P. &Palefsky, J. Burden of human papillomavirus infection and related comorbidities in men: implications for research, disease prevention and health promotion among Hispanic men. P. R. Health Sci. J. 29, 232-240 (2010
138. Faridi, R., Zahra, A., Khan, K. &Idrees, M. Oncogenic potential of Human Papillomavirus (HPV) and its relation with cervical cancer. Virol. J. 8, 269 (2011
139. Bouvard, V. et al. A review of human carcinogens-Part B: biological agents. Lancet Oncol. 10, 321-322 (2009
140. Foresta, C. et al. Mechanism of human papillomavirus binding to human spermatozoa and fertilizing ability of infected spermatozoa. PLoS ONE 6, e15036 (2011
141. Dunne, E. F., Nielson, C. M., Stone, K. M., Markowitz, L. E. &Giuliano, A. R. Prevalence of HPV infection among men: A systematic review of the literature. J. Infect. Dis. 194, 1044-1057 (2006
142. Goldstone, S. E. et al. Quadrivalent HPV vaccine efficacy against disease related to vaccine and non-vaccine HPV types in males. Vaccine 31, 3849-3855 (2013
143. Wortley, P. M., Hammett, T. A. &Fleming, P. L. Donor insemination and human immunodeficiency virus transmission. Obstet. Gynecol. 91, 515-518 (1998
144. Berry, W. R., Gottesfeld, R. L., Alter, H. J. &Vierling, J. M. Transmission of hepatitis B virus by artificial insemination. JAMA 257, 1079-1081 (1987
145. Moore, D. E. et al. Transmission of genital herpes by donor insemination. JAMA 261, 3441-3443 (1989
146. Laprise, C., Trottier, H., Monnier, P., Coutlee, F. &Mayrand, M. H. Prevalence of human papillomaviruses in semen: a systematic review and meta-Analysis. Hum. Reprod. 29, 640-651 (2014
147. Kaspersen, M. D. et al. Identification of multiple HPV types on spermatozoa from human sperm donors. PLoS ONE 6, e18095 (2011
148. Comar, M. et al. Association between the JC polyomavirus infection and male infertility. PLoS ONE 7, e42880 (2012
149. Yang, Y., Jia, C. W., Ma, Y. M., Zhou, L. Y. &Wang, S. Y. Correlation between HPV sperm infection and male infertility. Asian J. Androl. 15, 529-532 (2013
150. Lai, Y. M. et al. The effect of human papillomavirus infection on sperm cell motility. Fertil. Steril. 67, 1152-1155 (1997
151. Foresta, C. et al. Clinical and prognostic significance of human papillomavirus DNA in the sperm or exfoliated cells of infertile patients and subjects with risk factors. Fertil. Steril. 94, 1723-1727 (2010
152. Foresta, C. et al. Human papillomavirus found in sperm head of young adult males affects the progressive motility. Fertil. Steril. 93, 802-806 (2010
153. Foresta, C. et al. Human papillomavirus proteins are found in peripheral blood and semen Cd20+ and Cd56+ cells during Hpv-16 semen infection. BMC Infect. Dis. 13, 593 (2013
154. Kyo, S. et al. Detection of high-risk human papillomavirus in the cervix and semen of sex partners. J. Infect. Dis. 170, 682-685 (1994
155. Lai, Y. M., Yang, F. P. &Pao, C. C. Human papillomavirus deoxyribonucleic acid and ribonucleic acid in seminal plasma and sperm cells. Fertil. Steril. 65, 1026-1030 (1996
156. Rintala, M. A., Grenman, S. E., Pollanen, P. P., Suominen, J. J. &Syrjanen, S. M. Detection of high-risk HPV DNA in semen and its association with the quality of semen. Int. J. STD AIDS 15, 740-743 (2004
157. Perez-Andino, J., Buck, C. B. &Ribbeck, K. Adsorption of human papillomavirus 16 to live human sperm. PLoS ONE 4, e5847 (2009
158. Rintala, M. A., Pollanen, P. P., Nikkanen, V. P., Grenman, S. E. &Syrjanen, S. M. Human papillomavirus DNA is found in the vas deferens. J. Infect. Dis. 185, 1664-1667 (2002
159. Keck, C., Gerber-Schafer, C., Clad, A., Wilhelm, C. &Breckwoldt, M. Seminal tract infections: impact on male fertility and treatment options. Hum. Reprod. Update 4, 891-903 (1998
160. Roperto, S. et al. PBMCs are additional sites of productive infection of bovine papillomavirus type 2. J. Gen. Virol. 92, 1787-1794 (2011
161. Barzon, L., Militello, V., Pagni, S. &Palu, G. Comparison of INNO-LiPA genotyping extra and hybrid capture 2 assays for detection of carcinogenic human papillomavirus genotypes. J. Clin. Virol. 55, 256-261 (2012
162. Garolla, A. et al. Human papillomavirus sperm infection and assisted reproduction: a dangerous hazard with a possible safe solution. Hum. Reprod. 27, 967-973 (2012
163. Carter, J. J. et al. Comparison of human papillomavirus types 16, 18, and 6 capsid antibody responses following incident infection. J. Infect. Dis. 181, 1911-1919 (2000
164. Weyn, C. et al. Evidence of human papillomavirus in the placenta. J. Infect. Dis. 203, 341-343 (2011
165. Dana, A. et al. Pregnancy outcomes from the pregnancy registry of a human papillomavirus type 6/11/16/18 vaccine. Obstet. Gynecol. 114, 1170-1178 (2009
166. Perino, A. et al. Human papillomavirus infection in couples undergoing in vitro fertilization procedures: impact on reproductive outcomes. Fertil. Steril. 95, 1845-1848 (2011
167. Sabatte, J. et al. Semen clusterin is a novel DC-SIGN ligand. J. Immunol. 187, 5299-5309 (2011
168. McGowan, J. P. &Shah, S. S. Prevention of perinatal HIV transmission during pregnancy. J. Antimicrob. Chemother. 46, 657-668 (2000
169. Galvin, S. R. &Cohen, M. S. The role of sexually transmitted diseases in HIV transmission. Nat. Rev. Microbiol. 2, 33-42 (2004
170. Pilcher, C. D. et al. HIV in body fluids during primary HIV infection: implications for pathogenesis, treatment and public health. AIDS 15, 837-845 (2001
171. Gupta, P. et al. Human immunodeficiency virus type 1 shedding pattern in semen correlates with the compartmentalization of viral Quasi species between blood and semen. J. Infect. Dis. 182, 79-87 (2000
172. Shattock, R. J. &Moore, J. P. Inhibiting sexual transmission of HIV-1 infection. Nat. Rev. Microbiol. 1, 25-34 (2003
173. Lederman, M. M., Offord, R. E. &Hartley, O. Microbicides and other topical strategies to prevent vaginal transmission of HIV. Nat. Rev. Immunol. 6, 371-382 (2006
174. Hladik, F. &McElrath, M. J. Setting the stage: host invasion by HIV. Nat. Rev. Immunol. 8, 447-457 (2008
175. Ceballos, A. et al. Spermatozoa capture HIV-1 through heparan sulfate and efficiently transmit the virus to dendritic cells. J. Exp. Med. 206, 2717-2733 (2009
176. Anderson, J. A. et al. HIV-1 Populations in semen arise through multiple mechanisms. PLoS Pathog. 6, e1001053 (2010
177. Berlier, W. et al. Amount of seminal IL-1beta positively correlates to HIV-1 load in the semen of infected patients. J. Clin. Virol. 36, 204-207 (2006
178. Cardona-Maya, W., Lopez-Herrera, A., Velilla-Hernandez, P., Rugeles, M. T. &Cadavid, A. P. The role of mannose receptor on HIV-1 entry into human spermatozoa. Am. J. Reprod. Immunol. 55, 241-245 (2006
179. Bagasra, O., Freund, M., Weidmann, J. &Harley, G. Interaction of human immunodeficiency virus with human sperm in vitro. J. Acquir. Immune Defic. Syndr. 1, 431-435 (1988
180. Bagasra, O. et al. Detection of HIV-1 proviral DNA in sperm from HIV-1-infected men. AIDS 8, 1669-1674 (1994
181. Barboza, J. M. et al. Use of atomic force microscopy to reveal sperm ultrastructure in HIV-patients on highly active antiretroviral therapy. Arch. Androl. 50, 121-129 (2004
182. Nuovo, G. J. et al. HIV-1 nucleic acids localize to the spermatogonia and their progeny. A study by polymerase chain reaction in situ hybridization. Am. J. Pathol. 144, 1142-1148 (1994
183. Muciaccia, B. et al. Presence and cellular distribution of HIV in the testes of seropositive subjects: an evaluation by in situ PCR hybridization. FASEB J. 12, 151-163 (1998
184. Muciaccia, B. et al. Testicular germ cells of HIV-seropositive asymptomatic men are infected by the virus. J. Reprod. Immunol. 41, 81-93 (1998
185. Shevchuk, M. M., Nuovo, G. J. &Khalife, G. HIV in testis: quantitative histology and HIV localization in germ cells. J. Reprod. Immunol. 41, 69-79 (1998
186. Shehu-Xhilaga, M. et al. The testis and epididymis are productively infected by SIV and SHIV in juvenile macaques during the post-Acute stage of infection. Retrovirology 4, 7 (2007
187. van Leeuwen, E. et al. Effects of antiretroviral therapy on semen quality. AIDS 22, 637-642 (2008
188. Dondero, F. et al. Semen analysis in HIV seropositive men and in subjects at high risk for HIV infection. Hum. Reprod. 11, 765-768 (1996
189. Nicopoullos, J. D., Almeida, P. A., Ramsay, J. W. &Gilling-Smith, C. The effect of human immunodeficiency virus on sperm parameters and the outcome of intrauterine insemination following sperm washing. Hum. Reprod. 19, 2289-2297 (2004
190. Pavili, L. et al. Decrease of mitochondrial DNA level in sperm from patients infected with human immunodeficiency virus-1 linked to nucleoside analogue reverse transcriptase inhibitors. Fertil. Steril. 94, 2151-2156 (2010
191. Kehl, S. et al. HIV-infection and modern antiretroviral therapy impair sperm quality. Arch. Gynecol. Obstet. 284, 229-233 (2011
192. Dulioust, E. et al. Semen alterations in HIV-1 infected men. Hum. Reprod. 17, 2112-2118 (2002
193. Mencaglia, L. et al. ICSI for treatment of human immunodeficiency virus and hepatitis C virus-serodiscordant couples with infected male partner. Hum. Reprod. 20, 2242-2246 (2005
194. Bujan, L. et al. Decreased semen volume and spermatozoa motility in HIV-1-infected patients under antiretroviral treatment. J. Androl. 28, 444-452 (2007
195. Melo, M. A. et al. Human immunodeficiency type-1 virus (HIV-1) infection in serodiscordant couples (SDCs) does not have an impact on embryo quality or intracytoplasmic sperm injection (ICSI) outcome. Fertil. Steril. 89, 141-150 (2008
196. Vandermaelen, A. &Englert, Y. Human immunodeficiency virus serodiscordant couples on highly active antiretroviral therapies with undetectable viral load: conception by unprotected sexual intercourse or by assisted reproduction techniques? Hum. Reprod. 25, 374-379 (2010
197. Conrady, C. D., Jones, H., Zheng, M. &Carr, D. J. A functional type I interferon pathway drives resistance to cornea herpes simplex virus type 1 infection by recruitment of leukocytes. J. Biomed. Res. 25, 111-119 (2011
198. Wald, A. et al. Reactivation of genital herpes simplex virus type 2 infection in asymptomatic seropositive persons. N. Engl. J. Med. 342, 844-850 (2000
199. Zuckerman, R. A. et al. HSV suppression reduces seminal HIV-1 levels in HIV-1/HSV-2 co-infected men who have sex with men. AIDS 23, 479-483 (2009
200. Neofytou, E., Sourvinos, G., Asmarianaki, M., Spandidos, D. A. &Makrigiannakis, A. Prevalence of human herpes virus types 1-7 in the semen of men attending an infertility clinic and correlation with semen parameters. Fertil. Steril. 91, 2487-2494 (2009
201. Bocharova, E. N. et al. Detection of herpes simplex virus genomic DNA in spermatozoa of patients with fertility disorders by in situ hybridization. Dokl. Biol. Sci. 412, 82-86 (2007
202. DeTure, F. A., Drylie, D. M., Kaufman, H. E. &Centifanto, Y. N. Herpesvirus type 2: isolation from seminal vesicle and testes. Urology 7, 541-544 (1976
203. Huttner, K. M., Pudney, J., Milstone, D. S., Ladd, D. &Seidman, J. G. Flagellar and acrosomal abnormalities associated with testicular HSV-tk expression in the mouse. Biol. Reprod. 49, 251-261 (1993
204. Cai, L. Y. et al. HSV type 1 thymidine kinase protein accumulation in round spermatids induces male infertility by spermatogenesis disruption and apoptotic loss of germ cells. Reprod. Toxicol. 27, 14-21 (2009
205. el Borai, N. et al. Detection of herpes simplex DNA in semen and menstrual blood of individuals attending an infertility clinic. J. Obstet. Gynaecol. Res. 23, 17-24 (1997
206. Erles, K. et al. DNA of adeno-Associated virus (AAV) in testicular tissue and in abnormal semen samples. Hum. Reprod. 16, 2333-2337 (2001
207. Abdulmedzhidova, A. G. et al. Asymptomatic genital herpes infection and infertility in males [Russian]. Urologiia 56-59 (2007
208. Wu, K. H. et al. Infection of cytomegalovirus and herpes simplex virus and morphology of the infected spermatogenic cells in infertile men [Chinese]. Zhonghua Nan Ke Xue 13, 1075-1079 (2007
209. Klimova, R. R. et al. Herpes simplex virus and cytomegalovirus in male ejaculate: herpes simplex virus is more frequently encountered in idiopathic infertility and correlates with the reduction in sperm parameters [Russian]. Vopr. Virusol. 55, 27-31 (2010
210. Pilikian, S., Guerin, J. F., Czyba, J. C. &Pinatel, M. C. Study of different components in spermatic function after failure of in vitro fertilization [French]. Contracept. Fertil. Sex. 21, 865-868 (1993
211. Aydin, S. et al. Failure of artificial insemination of husband's semen in the treatment of male infertility. Int. Urol. Nephrol. 28, 117-122 (1996
212. Kaspersen, M. D. &Hollsberg, P. Seminal shedding of human herpesviruses. Virol. J. 10, 226 (2013
213. Zea-Mazo, J. W., Negrette-Mejia, Y. A. &Cardona-Maya, W. Virus of sexual transmission: semen and virus relationship [Spanish]. Actas Urol. Esp. 34, 845-853 (2010
214. Qian, W. P. et al. Rapid quantification of semen hepatitis B virus DNA by real-time polymerase chain reaction. World J. Gastroenterol. 11, 5385-5389 (2005
215. Hadchouel, M. et al. Presence of HBV DNA in spermatozoa: a possible vertical transmission of HBV via the germ line. J. Med. Virol. 16, 61-66 (1985
216. Huang, J. M. et al. Studies on the integration of hepatitis B virus DNA sequence in human sperm chromosomes. Asian J. Androl. 4, 209-212 (2002
217. Vicari, E. et al. Sperm output in patients with primary infertility and hepatitis B or C virus; negative influence of HBV infection during concomitant varicocele. Minerva Med. 97, 65-77 (2006
218. Kang, X. et al. Effects of hepatitis B virus S. protein exposure on sperm membrane integrity and functions. PLoS ONE 7, e33471 (2012
219. Xu, X. The possible role of sperm in family HBV infection [Chinese]. Zhonghua Liu Xing Bing Xue Za Zhi 13, 337-339 (1992
220. Otedo, A. E., Mc'Ligeyo, S. O., Okoth, F. A. &Kayima, J. K. Seroprevalence of hepatitis B and C in maintenance dialysis in a public hospital in a developing country. S. Afr. Med. J. 93, 380-384 (2003
221. Zhao, H., Jiang, P. &Yin, H. Study on the contents of HBV DNA in sera of patients with hepatic diseases by QPCR technique [Chinese]. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 12, 367-369 (1998
222. Harvey, H. A. et al. Gonococcal lipooligosaccharide is a ligand for the asialoglycoprotein receptor on human sperm. Mol. Microbiol. 36, 1059-1070 (2000
223. Zhou, X. P. et al. Comparison of semen quality and outcome of assisted reproductive techniques in Chinese men with and without hepatitis B. Asian J. Androl. 13, 465-469 (2011
224. Ali, B. A., Huang, T. H. &Xie, Q. D. Detection and expression of hepatitis B virus X gene in one and two-cell embryos from golden hamster oocytes in vitro fertilized with human spermatozoa carrying HBV DNA. Mol. Reprod. Dev. 70, 30-36 (2005
225. Xiong, X. Y., Liu, X. &Chen, Y. D. Expression and immunoreactivity of HCV/HBV epitopes. World J. Gastroenterol. 11, 6440-6444 (2005
226. Ali, B. A., Huang, T. H., Salem, H. H. &Xie, Q. D. Expression of hepatitis B virus genes in early embryonic cells originated from hamster ova and human spermatozoa transfected with the complete viral genome. Asian J. Androl. 8, 273-279 (2006
227. Lee, V. C., Ng, E. H., Yeung, W. S. &Ho, P. C. Impact of positive hepatitis B surface antigen on the outcome of IVF treatment. Reprod. Biomed. Online 21, 712-717 (2010
228. Aitken, R. J., Harkiss, D. &Buckingham, D. W. Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol. Reprod. Dev. 35, 302-315 (1993
229. Wang, X. et al. Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study. Fertil. Steril. 80 (Suppl. 2), 844-850 (2003
230. Wu, J. N. et al. Caspase inhibition augmented oridonin-induced cell death in murine fibrosarcoma l929 by enhancing reactive oxygen species generation. J. Pharmacol. Sci. 108, 32-39 (2008
231. Bourlet, T. et al. Detection and characterization of hepatitis C virus RNA in seminal plasma and spermatozoon fractions of semen from patients attempting medically assisted conception. J. Clin. Microbiol. 40, 3252-3255 (2002
232. Cassuto, N. G. et al. A modified RT-PCR technique to screen for viral RNA in the semen of hepatitis C virus-positive men. Hum. Reprod. 17, 3153-3156 (2002
233. Nguyen, O., Sheppeard, V., Douglas, M. W., Tu, E. &Rawlinson, W. Acute hepatitis C infection with evidence of heterosexual transmission. J. Clin. Virol. 49, 65-68 (2010
234. Terrault, N. A. Sexual activity as a risk factor for hepatitis C. Hepatology 36, S99-S105 (2002
235. Durazzo, M. et al. Alterations of seminal and hormonal parameters: An extrahepatic manifestation of HCV infection? World J. Gastroenterol. 12, 3073-3076 (2006
236. Alter, M. J. et al. Importance of heterosexual activity in the transmission of hepatitis B and non-A, non-B hepatitis. JAMA 262, 1201-1205 (1989
237. Piazza, M. et al. Sexual transmission of the hepatitis C virus and efficacy of prophylaxis with intramuscular immune serum globulin. A randomized controlled trial. Arch. Intern. Med. 157, 1537-1544 (1997
238. Vandelli, C. et al. Lack of evidence of sexual transmission of hepatitis C among monogamous couples: results of a 10-year prospective follow-up study. Am. J. Gastroenterol. 99, 855-859 (2004
239. Tahan, V. et al. Sexual transmission of HCV between spouses. Am. J. Gastroenterol. 100, 821-824 (2005
240. Sexually transmitted diseases, treatment guidelines, 2010, Hepatitis C. Centers for Disease Control and Prevention [online], http://www.cdc.gov/std/treatment/2010/hepC.htm (2010
241. Levy, R. et al. Transmission risk of hepatitis C virus in assisted reproductive techniques. Hum. Reprod. 15, 810-816 (2000
242. Levy, R. et al. Pregnancy after safe IVF with hepatitis C virus RNA-positive sperm. Hum. Reprod. 17, 2650-2653 (2002
243. Filippini, P. et al. Does HIV infection favor the sexual transmission of hepatitis C? Sex. Transm. Dis. 28, 725-729 (2001
244. Briat, A. et al. Hepatitis C virus in the semen of men coinfected with HIV-1: prevalence and origin. AIDS 19, 1827-1835 (2005
245. Halfon, P. et al. Medically assisted procreation and transmission of hepatitis C virus: absence of HCV RNA in purified sperm fraction in HIV co-infected patients. AIDS 20, 241-246 (2006
246. Bourlet, T. et al. Prospective evaluation of the threat related to the use of seminal fractions from hepatitis C virus-infected men in assisted reproductive techniques. Hum. Reprod. 24, 530-535 (2009
247. Hofny, E. R. et al. Semen and hormonal parameters in men with chronic hepatitis C infection. Fertil. Steril. 95, 2557-2559 (2011
248. Savasi, V., Oneta, M., Parrilla, B. &Cetin, I. Should HCV discordant couples with a seropositive male partner be treated with assisted reproduction techniques (ART)? Eur. J. Obstet. Gynecol. Reprod. Biol. 167, 181-184 (2013
249. Goldberg-Bittman, L. et al. Random aneuploidy in chronic hepatitis C patients. Cancer Genet. Cytogenet. 180, 20-23 (2008
250. Devaux, A. et al. Hepatitis C virus detection in follicular fluid and culture media from HCV+ women, and viral risk during IVF procedures. Hum. Reprod. 18, 2342-2349 (2003
251. Abou-Setta, A. M. Transmission risk of hepatitis C virus via semen during assisted reproduction: how real is it? Hum. Reprod. 19, 2711-2717 (2004
252. Sifer, C. et al. Effects of hepatitis C virus on the apoptosis percentage of granulosa cells in vivo in women undergoing IVF: preliminary results. Hum. Reprod. 17, 1773-1776 (2002
253. Papaxanthos-Roche, A. et al. PCR-detected hepatitis C virus RNA associated with human zona-intact oocytes collected from infected women for ART. Hum. Reprod. 19, 1170-1175 (2004
254. Savasi, V. et al. Hepatitis C virus RNA detection in different semen fractions of HCV/HIV-1 co-infected men by nested PCR. Eur. J. Obstet. Gynecol. Reprod. Biol. 151, 52-55 (2010
255. Foster, G. R. Past, present, and future hepatitis C treatments. Semin. Liver Dis. 24 (Suppl. 2), 97-104 (2004
256. Gimenes, F. et al. Sensitive simultaneous detection of seven sexually transmitted agents in semen by multiplex-PCR and of HPV by single PCR. PLoS ONE 9, e98862 (2014
257. Spector, S. A., Merrill, R., Wolf, D. &Dankner, W. M. Detection of human cytomegalovirus in plasma of AIDS patients during acute visceral disease by DNA amplification. J. Clin. Microbiol. 30, 2359-2365 (1992
258. Eggert-Kruse, W., Reuland, M., Johannsen, W., Strowitzki, T. &Schlehofer, J. R. Cytomegalovirus (CMV) infection-related to male and/or female infertility factors? Fertil. Steril. 91, 67-82 (2009
259. Roback, J. D. et al. Multicenter evaluation of PCR methods for detecting CMV DNA in blood donors. Transfusion 41, 1249-1257 (2001
260. Diafouka, F., Foulongne, V., Hauhouot-Attoungbre, M. L., Monnet, D. &Segondy, M. Cytomegalovirus DNA in semen of men seeking fertility evaluation in Abidjan, Cote d'Ivoire. Eur. J. Clin. Microbiol. Infect. Dis. 26, 295-296 (2007
261. McGowan, M. P., Hayes, K., Kovacs, G. T. &Leydon, J. A. Prevalence of cytomegalovirus and herpes simplex virus in human semen. Int. J. Androl. 6, 331-336 (1983
262. Levy, R. et al. Detection of cytomegalovirus in semen from a population of men seeking infertility evaluation. Fertil. Steril. 68, 820-825 (1997
263. Pallier, C. et al. Herpesvirus, cytomegalovirus, human sperm and assisted fertilization. Hum. Reprod. 17, 1281-1287 (2002
264. Dalton, A. D. &Harcourt-Webster, J. N. The histopathology of the testis and epididymis in AIDS-A post-mortem study. J. Pathol. 163, 47-52 (1991
265. Kimura, M., Maekura, S., Satou, T. &Hashimoto, S. Cytomegaloviral inclusions detected in the seminal vesicle, ductus deferens and lungs in an autopsy case of lung cancer [Japanese]. Rinsho Byori 41, 1059-1062 (1993
266. Mastroianni, A., Coronado, O., Manfredi, R., Chiodo, F. &Scarani, P. Acute cytomegalovirus prostatitis in AIDS. Genitourin. Med. 72, 447-448 (1996
267. Lang, D. J., Kummer, J. F. &Hartley, D. P. Cytomegalovirus in semen. Persistence and demonstration in extracellular fluids. N. Engl. J. Med. 291, 121-123 (1974
268. Naumenko, V. A. et al. Detection of human cytomegalovirus in motile spermatozoa and spermatogenic cells in testis organotypic culture. Herpesviridae 2, 7 (2011
269. Naumenko, V. et al. Detection and quantification of human herpes viruses types 4-6 in sperm samples of patients with fertility disorders and chronic inflammatory urogenital tract diseases. Andrology 2, 687-694 (2014
270. McClelland, R. S. Trichomonas vaginalis infection: can we afford to do nothing? J. Infect. Dis. 197, 487-489 (2008
271. Harp, D. F. &Chowdhury, I. Trichomoniasis: evaluation to execution. Eur. J. Obstet. Gynecol. Reprod. Biol. 157, 3-9 (2011
272. Sood, S. &Kapil, A. An update on Trichomonas vaginalis. Indian J. Sex. Dis. 29, 7-14 (2008
273. Mitteregger, D. et al. High detection rate of Trichomonas vaginalis in benign hyperplastic prostatic tissue. Med. Microbiol. Immunol. 201, 113-116 (2012
274. Krieger, J. N. Trichomoniasis in men: old issues and new data. Sex. Transm. Dis. 22, 83-96 (1995
275. Watson-Jones, D. et al. High prevalence of trichomoniasis in rural men in Mwanza, Tanzania: results from a population based study. Sex. Transm. Infect. 76, 355-362 (2000
276. Carlton, J. M. et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207-212 (2007
277. Soper, D. Trichomoniasis: under control or undercontrolled? Am. J. Obstet. Gynecol. 190, 281-290 (2004
278. Sommer, U. et al. Identification of Trichomonas vaginalis cysteine proteases that induce apoptosis in human vaginal epithelial cells. J. Biol. Chem. 280, 23853-23860 (2005
279. Sutcliffe, S., Neace, C., Magnuson, N. S., Reeves, R. &Alderete, J. F. Trichomonosis, a common curable STI, and prostate carcinogenesis-A proposed molecular mechanism. PLoS Pathog. 8, e1002801 (2012
280. Gomez, C., Esther Ramirez, M., Calixto-Galvez, M., Medel, O. &Rodriguez, M. A. Regulation of gene expression in protozoa parasites. J. Biomed. Biotechnol. 2010, 726045 (2010
281. Westrop, G. D., Goodall, G., Mottram, J. C. &Coombs, G. H. Cysteine biosynthesis in Trichomonas vaginalis involves cysteine synthase utilizing O-phosphoserine. J. Biol. Chem. 281, 25062-25075 (2006
282. Yadav, M., Gupta, I. &Malla, N. Kinetics of immunoglobulin G, M, A and IgG subclass responses in experimental intravaginal trichomoniasis: prominence of IgG1 response. Parasite Immunol. 27, 461-467 (2005
283. Crouch, M. L., Benchimol, M. &Alderete, J. F. Binding of fibronectin by Trichomonas vaginalis is influenced by iron and calcium. Microb. Pathog. 31, 131-144 (2001
284. Alderete, J. F., Benchimol, M., Lehker, M. W. &Crouch, M. L. The complex fibronectin-Trichomonas vaginalis interactions and Trichomonosis. Parasitol. Int. 51, 285-292 (2002
285. Lubick, K. J. &Burgess, D. E. Purification and analysis of a phospholipase A2-like lytic factor of Trichomonas vaginalis. Infect. Immun. 72, 1284-1290 (2004
286. Singh, B. N. et al. Structural details and composition of Trichomonas vaginalis lipophosphoglycan in relevance to the epithelial immune function. Glycoconj. J. 26, 3-17 (2009
287. Hobbs, M. M., Sena, A. C., Swygard, H. &Schwebke, J. R. in Sexually transmitted diseases. 4th edn Ch. 43 (eds Holmes, K. K. et al.) 771-794 (McGraw-Hill, 2008
288. Ryu, J. S. et al. Production of interleukin-8 by human neutrophils stimulated with Trichomonas vaginalis. Infect. Immun. 72, 1326-1332 (2004
289. Kucknoor, A. S., Mundodi, V. &Alderete, J. F. The proteins secreted by Trichomonas vaginalis and vaginal epithelial cell response to secreted and episomally expressed AP65. Cell. Microbiol. 9, 2586-2597 (2007
290. Tan, C. H., Loh, P. T., Yang, W. S. &Chan, C. M. Mycophenolate mofetil in the treatment of IgA nephropathy: a systematic review. Singapore Med. J. 49, 780-785 (2008
291. Fichorova, R. N. Impact of T. vaginalis infection on innate immune responses and reproductive outcome. J. Reprod. Immunol. 83, 185-189 (2009
292. Han, I. H., Park, S. J., Ahn, M. H. &Ryu, J. S. Involvement of mast cells in inflammation induced by Trichomonas vaginalis via crosstalk with vaginal epithelial cells. Parasite Immunol. 34, 8-14 (2012
293. Cowan, M. J., Coll, T. &Shelhamer, J. H. Polyamine-mediated reduction in human airway epithelial migration in response to wounding is PGE2 dependent through decreases in COX-2 and cPLA2 protein levels. J. Appl. Physiol. (1985) 101, 1127-1135 (2006
294. Garcia, A. F., Benchimol, M. &Alderete, J. F. Trichomonas vaginalis polyamine metabolism is linked to host cell adherence and cytotoxicity. Infect. Immun. 73, 2602-2610 (2005
295. Gardner, W. A. Jr, Culberson, D. E. &Bennett, B. D. Trichomonas vaginalis in the prostate gland. Arch. Pathol. Lab. Med. 110, 430-432 (1986
296. Fitzpatrick, J. M. The natural history of benign prostatic hyperplasia. BJU Int. 97 (Suppl. 2), 3-6 (2006