Affect of Trichomonas vaginalis infection on male reproductive system and its mechanisms

doi:10.12140/j.issn.1000-7423.2021.04.018

Abstract

Abstract:

Trichomonas vaginalis is a type of flagellated protozoan and the most common sexually transmitted pathogens in the world. T. vaginalis mainly parasitizes in the female vagina, leading to trichomonal vaginitis. In addition, T. vaginalis can also infect males, and the parasites may retrograde to the bladder, prostate, seminal vesicle, testis, epididymis and other tissues, through the urogenital tract, thus causing serious damage to sperm cells or other tissues; causing urethritis, prostatitis, prostate cancer, asthenospermia or azoospermia, eventually affecting the male fertility. However, T. vaginalis infection in males often presents mild or no clinical symptoms, resulting in ignorance of the infection. In this paper, we review the related mechanisms underlying the T. vaginalis infection-induced abnormal sperm, testicular and prostate functions, and thereby male infertility.

Key words: Trichomonas vaginalis, Infertility, Sperm, Prostate, Testicles

CLC Number:

R382.211

DUAN Yu-juan, LI Peng-ju, SANG Yu-hui, WU Pu-cheng, SHANG Yu-jia, HAO Li-xia, WANG Shuai, LI Xiang-rui, ZHANG Zhen-chao. Affect of Trichomonas vaginalis infection on male reproductive system and its mechanisms[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2021, 39(4): 532-536.

References 58

[1]	Su RY, Ho LJ, Yang HY, et al. Association between Trichomonas vaginalis infection and cervical lesions: a population-based, nested case-control study in Taiwan[J]. Parasitol Res, 2020, 119(8):2649-2657. doi: 10.1007/s00436-020-06759-4
[2]	Rowley J, Vander Hoorn S, Korenromp E, et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016[J]. Bull World Health Organ, 2019, 97(8):548-562. doi: 10.2471/BLT.18.228486
[3]	World Health Organization. Report on global sexually transmitted infection surveillance[R]. Geneva: WHO, 2018.
[4]	Zhao NN. Study on leucorrhea examination and infection rate in trichomoniasis fungal vaginitis[J]. Med Forum, 2021, 25(1):102-103. (in Chinese)
	(赵男男. 滴虫霉菌性阴道炎患者白带检验及感染率动态研究[J]. 基层医学论坛, 2021, 25(1):102-103.)
[5]	Chen Y, Liu SL, Ma DX, et al. Analysis of 19 342 cases of Trichomonas vaginalis[J]. J Trop Med, 2019, 19(9):1177-1179. (in Chinese)
	(陈杨, 刘素伶, 马丹霞, 等. 19 342例阴道毛滴虫检查结果分析[J]. 热带医学杂志, 2019, 19(9):1177-1179.)
[6]	Bi H. Leucorrhea test and dynamic analysis of infection rate in patients with trichomonad fungal vaginitis[J]. J Clin Med Lit, 2016, 3(47):9323. (in Chinese)
	(毕恒. 滴虫霉菌性阴道炎患者白带检验及感染率动态分析[J]. 临床医药文献电子杂志, 2016, 3(47):9323.)
[7]	Zhang ZC, Kang LX, Wang WJ, et al. Prevalence and genetic diversity of Trichomonas vaginalis clinical isolates in a targeted population in Xinxiang City, Henan Province, China[J]. Parasit Vectors, 2018, 11(1):124. doi: 10.1186/s13071-018-2753-4
[8]	He YF. Analysis of Trichomonas vaginalis infection in gynecology and preventive measures[J]. Chin J Nosocomiol, 2012, 22(6):1205-1206. (in Chinese)
	(何燕妃. 妇科阴道毛滴虫感染分析及预防措施[J]. 中华医院感染学杂志, 2012, 22(6):1205-1206.)
[9]	Zhu RY, Zhu YF, Fu RN, et al. Investigation and analysis of Trichomonas vaginalis infection in middle-aged and elderly patients with vaginitis[J]. Prog Mod Biomed, 2020, 20(18):3478-3481, 3557. (in Chinese)
	(朱荣英, 朱艳芳, 付蕊宁, 等. 中老年阴道炎患者阴道毛滴虫感染状况调查分析[J]. 现代生物医学进展, 2020, 20(18):3478-3481, 3557.)
[10]	ACOG Committee on Practice Bulletins--Gynecology. ACOG Practice Bulletin. Clinical management guidelines for obstetrician-gynecologists, Number 72, May 2006: Vaginitis[J]. Obstet Gynecol, 2006, 107(5):1195-1206. doi: 10.1097/00006250-200605000-00049
[11]	Meites E, Gaydos CA, Hobbs MM, et al. A review of evidence-based care of symptomatic trichomoniasis and asymptomatic Trichomonas vaginalis infections[J]. Clin Infect Dis, 2015, 61(Suppl 8):S837-S848. doi: 10.1093/cid/civ738
[12]	Krieger JN. Trichomoniasis in men: old issues and new data[J]. Sex Transm Dis, 1995, 22(2):83-96. pmid: 7624817
[13]	Aquino MFK, Hinderfeld AS, Simoes-Barbosa A. Trichomonas vaginalis[J]. Trends Parasitol, 2020, 36(7):646-647. doi: 10.1016/j.pt.2020.01.010
[14]	Xu ZX. Influence of Trichomonas vaginalis infection on semen parameters[J]. J Henan Univ Med Sci, 2005, 24(2):59-60. (in Chinese)
	(徐志喜. 阴道毛滴虫感染对精液各参数的影响[J]. 河南大学学报(医学版), 2005, 24(2):59-60.)
[15]	Roh J, Lim YS, Seo MY, et al. The secretory products of Trichomonas vaginalis decrease fertilizing capacity of mice sperm in vitro[J]. Asian J Androl, 2015, 17(2):319-323. doi: 10.4103/1008-682X.145070
[16]	Han QJ, Liu JH. Effects of the metabolite of Trichomonas vaginalis on membrane function integrity of human sperm in vitro[J]. Chin J Misdiagnostics, 2005, 5(3):418-419. (in Chinese)
	(韩青江, 刘继红. 阴道毛滴虫代谢产物体外对精子膜功能的影响[J]. 中国误诊学杂志, 2005, 5(3):418-419.)
[17]	van Gerwen OT, Muzny CA. Recent advances in the epidemiology, diagnosis, and management of Trichomonas vaginalis infection[J]. F1000Res, 2019, 8: F1000FacultyRev-F1000Faculty1666.
[18]	Chen WL, Zhong XR, Chen JF, et al. An ultrastructural study on the process of spermatozoa phagocytosis by Trichomonas vaginalis[J]. J Chin Electron Microsc Soc, 1997, 16(1): 17-18, 21-22. (in Chinese)
	(陈文列, 钟秀容, 陈金富, 等. 阴道毛滴虫吞噬精子过程的超微结构观察[J]. 电子显微学报, 1997, 16(1): 17-18, 21-22.)
[19]	Chen WL, Zhong XR, Chen LY, et al. Ultrastructural cytochemistry of Trichomonas vaginalis[J]. J Chin Electron Microsc Soc, 1994, 13(5):346. (in Chinese)
	(陈文列, 钟秀容, 陈莲云, 等. 阴道毛滴虫的超微结构细胞化学研究[J]. 电子显微学报, 1994, 13(5):346.)
[20]	Benchimol M, de Andrade Rosa I, da Silva Fontes R, et al. Trichomonas adhere and phagocytose sperm cells: adhesion seems to be a prominent stage during interaction[J]. Parasitol Res, 2008, 102(4):597-604. pmid: 18043945
[21]	Tuttle JP Jr, Holbrook TW Jr, Derrick FC Jr. Interference of human spermatozoal motility by Trichomonas vaginalis[J]. J Urol, 1977, 118(6):1024-1025. doi: 10.1016/S0022-5347(17)58285-3
[22]	Wiwanitkit V. Counteraction during movement of spermatozoa by Trichomonas vaginalis observed by visual image analysis: a possible cause of female infertility[J]. Fertil Steril, 2008, 90(3):528-530. pmid: 17953953
[23]	Wiwanitkit V. Motion of spermatozoa by visual image analysis[J]. Sex Disabil, 2007, 25(3):151-154. doi: 10.1007/s11195-007-9041-0
[24]	Amos WB, Grimstone AV, Rothschild LJ, et al. Structure, protein composition and birefringence of the costa: a motile flagellar root fibre in the flagellate Trichomonas[J]. J Cell Sci, 1979, 35:139-164. pmid: 154523
[25]	Jarecki-Black JC, Lushbaugh WB, Golosov L, et al. Trichomonas vaginalis: preliminary characterization of a sperm motility inhibiting factor[J]. Ann Clin Lab Sci, 1988, 18(6):484-489. pmid: 3266454
[26]	Tash JS, Mann T. Adenosine 3’: 5’-cyclic monophosphate in relation to motility and senescence of spermatozoa[J]. Proc R Soc Lond B Biol Sci, 1973, 184(1074):109-114.
[27]	Cohen MS, Colin MJ, Golimbu M, et al. The effects of prostaglandins on sperm motility[J]. Fertil Steril, 1977, 28(1):78-85. pmid: 832720
[28]	Kranjcić-Zec I, Dzamić A, Mitrović S, et al. The role of parasites and fungi in secondary infertility[J]. Med Pregl, 2004, 57(1/2):30-32. doi: 10.2298/MPNS0402030K
[29]	Cai HZ, Chen WL, Zhong XR, et al. Study on enzymic location and metabolism of Trichomonas vaginalis[J]. Chin J Parasit Dis Control, 1993(4): 256-258, 323-324. (in Chinese)
	(蔡蕙珍, 陈文列, 钟秀容, 等. 阴道毛滴虫酶的定位与代谢的研究[J]. 中国寄生虫病防治杂志, 1993(4): 256-258, 323-324.)
[30]	Midlej V, Benchimol M. Trichomonas vaginalis kills and eats: evidence for phagocytic activity as a cytopathic effect[J]. Parasitology, 2010, 137(1):65-76. doi: 10.1017/S0031182009991041 pmid: 19723359
[31]	Lustig G, Ryan CM, Secor WE, et al. Trichomonas vaginalis contact-dependent cytolysis of epithelial cells[J]. Infect Immun, 2013, 81(5):1411-1419. doi: 10.1128/IAI.01244-12 pmid: 23429535
[32]	Mercer F, Johnson PJ. Trichomonas vaginalis: pathogenesis, symbiont interactions, and host cell immune responses[J]. Trends Parasitol, 2018, 34(8):683-693. doi: 10.1016/j.pt.2018.05.006
[33]	Bhakta SB, Moran JA, Mercer F. Neutrophil interactions with the sexually transmitted parasite Trichomonas vaginalis: implications for immunity and pathogenesis[J]. Open Biol, 2020, 10(9):200192. doi: 10.1098/rsob.200192
[34]	Im SJ, Han IH, Kim JH, et al. Inflammatory response of a prostate stromal cell line induced by Trichomonas vaginalis[J]. Parasite Immunol, 2016, 38(4):218-227. doi: 10.1111/pim.12308 pmid: 26832322
[35]	Daly JJ, Sherman JK, Green L, et al. Survival of Trichomonas vaginalis in human semen[J]. Genitourin Med, 1989, 65(2):106-108. pmid: 2787774
[36]	Pei F, Luo Q, Lv WJ, et al. Effect of chronic prostatitis on semen quality in men[J]. Chin J Reproductive Health, 2018, 29(3):262-265. (in Chinese)
	(裴峰, 罗倩, 吕文静, 等. 慢性前列腺炎对男性精液质量的影响[J]. 中国生育健康杂志, 2018, 29(3):262-265.)
[37]	Yuan HY, Ge B. Research progress of chronic prostatitis and male infertility mechanism[J]. Chin Pract Med, 2011, 6(4):256-258. (in Chinese)
	(袁宏毅, 葛波. 慢性前列腺炎与男性不育机制的研究进展[J]. 中国实用医药, 2011, 6(4):256-258.)
[38]	Bedwal RS, Bahuguna A. Zinc, copper and selenium in reproduction[J]. Experientia, 1994, 50(7):626-640. pmid: 8033970
[39]	Björndahl L, Kvist U. A model for the importance of zinc in the dynamics of human sperm chromatin stabilization after ejaculation in relation to sperm DNA vulnerability[J]. Syst Biol Reprod Med, 2011, 57(1/2):86-92. doi: 10.3109/19396368.2010.516306
[40]	Barratt CL, Aitken RJ, Björndahl L, et al. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications: a position report[J]. Hum Reprod, 2010, 25(4):824-838. doi: 10.1093/humrep/dep465
[41]	Alshahrani S, McGill J, Agarwal A. Prostatitis and male infertility[J]. J Reprod Immunol, 2013, 100(1):30-36. doi: 10.1016/j.jri.2013.05.004 pmid: 23938147
[42]	Najafi A, Chaechi Nosrati MR, Ghasemi E, et al. Is there association between Trichomonas vaginalis infection and prostate cancer risk?: asystematic review and meta-analysis[J]. Microb Pathog, 2019, 137:103752. doi: 10.1016/j.micpath.2019.103752
[43]	Han IH, Kim JH, Jang KS, et al. Inflammatory mediators of prostate epithelial cells stimulated with Trichomonas vaginalis promote proliferative and invasive properties of prostate cancer cells[J]. Prostate, 2019, 79(10):1133-1146. doi: 10.1002/pros.v79.10
[44]	Han IH, Song HO, Ryu JS. IL-6 produced by prostate epithelial cells stimulated with Trichomonas vaginalis promotes proliferation of prostate cancer cells by inducing M2 polarization of THP-1-derived macrophages[J]. PLoS Negl Trop Dis, 2020, 14(3):e0008126. doi: 10.1371/journal.pntd.0008126
[45]	Chung HY, Kim JH, Han IH, et al. Polarization of M2 macrophages by interaction between prostate cancer cells treated with Trichomonas vaginalis and adipocytes[J]. Korean J Parasitol, 2020, 58(3):217-227. doi: 10.3347/kjp.2020.58.3.217
[46]	Lee JJ, Moon HS, Lee TY, et al. PCR for diagnosis of male Trichomonas vaginalis infection with chronic prostatitis and urethritis[J]. Korean J Parasitol, 2012, 50(2):157-159. doi: 10.3347/kjp.2012.50.2.157
[47]	Inui A. Cancer anorexia-Cachexia syndrome: current issues in research and management[J]. CA Cancer J Clin, 2002, 52(2):72-91. doi: 10.3322/canjclin.52.2.72
[48]	Viviani S, Ragni G, Santoro A, et al. Testicular dysfunction in Hodgkin’s disease before and after treatment[J]. Eur J Cancer, 1991, 27(11):1389-1392. pmid: 1835853
[49]	Tsang SH, Peisch SF, Rowan B, et al. Association between Trichomonas vaginalis and prostate cancer mortality[J]. Int J Cancer, 2019, 144(10):2377-2380. doi: 10.1002/ijc.v144.10
[50]	Marous M, Huang WY, Rabkin CS, et al. Trichomonas vaginalis infection and risk of prostate cancer: associations by disease aggressiveness and race/ethnicity in the PLCO trial[J]. Cancer Causes Control, 2017, 28(8):889-898. doi: 10.1007/s10552-017-0919-6
[51]	Shui IM, Kolb S, Hanson C, et al. Trichomonas vaginalis infection and risk of advanced prostate cancer[J]. Prostate, 2016, 76(7):620-623. doi: 10.1002/pros.23153
[52]	Chen ZG, Guo B, Ma GC, et al. Clinical analysis of 5 cases of trichomonas urogenital infection[J]. Chin J Dermatovenereology, 2000, 14(6):404. (in Chinese)
	(陈宗淦, 郭宾, 马贵春, 等. 滴虫性泌尿生殖系感染5例临床分析[J]. 中国皮肤性病学杂志, 2000, 14(6):404.)
[53]	Gimenes F, Souza RP, Bento JC, et al. Male infertility: a public health issue caused by sexually transmitted pathogens[J]. Nat Rev Urol, 2014, 11(12):672-687.
[54]	La Vignera S, Vicari E, Condorelli RA, et al. Male accessory gland infection and sperm parameters (review)[J]. Int J Androl, 2011, 34(5 Pt 2):e330-e347. doi: 10.1111/j.1365-2605.2011.01200.x
[55]	Janssenswillen C, Tournaye H, Pierard D, et al. Microsurgical epididymal sperm aspiration with motile trophozoite cells but no spermatozoa[J]. Hum Reprod, 1997, 12(10):2217-2219. pmid: 9402284
[56]	Lloyd G, Case JR, De Frias D, et al. Trichomonas vaginalis orchitis with associated severe oligoasthenoteratospermia and hypogonadism[J]. J Urol, 2003, 170(3):924. doi: 10.1097/01.ju.0000080375.18547.cc
[57]	Naito M, Terayama H, Hirai S, et al. Experimental autoimmune orchitis as a model of immunological male infertility[J]. Med Mol Morphol, 2012, 45(4):185-189. doi: 10.1007/s00795-012-0587-2
[58]	Zhou PY. Systemic transmission of infection and infertility in male reproduction[J]. J Clin Dermatol, 2009, 38(3):198-200. (in Chinese)
	(周平玉. 男性生殖系统性传播感染与不育[J]. 临床皮肤科杂志, 2009, 38(3):198-200.)