Investigating ROS sources in male infertility: A common end for numerous pathways

Reproductive Toxicology

Volumn 34, Issue 3, 2012, Pages 298-307

  Lavranos, G ^a   Balla, M ^a   Tzortzopoulou, A ^a   Syriou, V ^a   Angelopoulou, R ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Antioxidants; Oxidative stress; Reactive oxygen species; Sperm; Toxicity

Indexed keywords

AMINOGLYCOSIDE; BLEOMYCIN; CATALASE; CHLORAMPHENICOL; CISPLATIN; ETHYLENE GLYCOL; ETOPOSIDE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; LACTATE DEHYDROGENASE; MALONALDEHYDE; PHOSPHATASE; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TETRACYCLINE DERIVATIVE;

AEROBIC METABOLISM; CELL INFILTRATION; CELL SURVIVAL; CELL VIABILITY; DIABETES MELLITUS; DNA FRAGMENTATION; ENZYME ACTIVITY; EPIDIDYMIS; GLYCEMIC CONTROL; GLYCOSYLATION; HUMAN; IONIZING RADIATION; LEUKOCYTE; LEUKOCYTOSIS; MALE; MALE GENITAL TRACT INFECTION; MALE INFERTILITY; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; RADIATION EXPOSURE; REVIEW; SIGNAL TRANSDUCTION; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TEMPERATURE; TESTIS; VARICOCELE;

ANIMALS; HUMANS; INFERTILITY, MALE; LEUKOCYTE COUNT; MALE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPERM CAPACITATION; SPERMATOZOA;

EID: 84865540531     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.06.007     Document Type: Review

References (129)

1. Makker K., Agarwal A., Sharma R. Oxidative stress and male infertility. Indian Journal of Medical Research 2009, 129(4):357-367.
2. Coccuzza M., Sikka S.C., Athayde K.S., Agarwal A. Clinical relevance of oxidative stress and sperm chromatin damage in male infertility: an evidence based analysis. International Braz J Urol 2007, 33(5):603-621.
3. Angelopoulou R., Lavranos G., Manolakou P. ROS in the aging male: model diseases with ROS-related pathophysiology. Reproductive Toxicology 2009, 28:167-171.
4. Deepinder F., Cocuzza M., Agarwal A. Should seminal oxidative stress measurement be offered routinely to men presenting for infertility evaluation?. Endocrine Practice 2008, 14(4):484-491.
5. Sikka S.C. Oxidative stress and role of antioxidants in normal and abnormal sperm function. Frontiers in Bioscience 1996, 1:e78-e86.
6. Ford W.C., Whittington K., Williams A.C. Reactive oxygen species in human sperm suspensions: production by leucocytes and the generation of NADPH to protect sperm against their effects. International Journal of Andrology 1997, 20(Suppl. 3):44-49.
7. Whittington K., Ford W.C. Relative contribution of leucocytes and of spermatozoa to reactive oxygen species production in human sperm suspensions. International Journal of Andrology 1999, 22(4):229-235.
8. Ford W.C. Regulation of sperm function by reactive oxygen species. Human Reproduction Update 2004, 10(5):387-399.
9. Henkel R., Kierspel E., Stalf T., Mehnert C., Menkveld R., Tinneberg H.R., et al. Effect of reactive oxygen species produced by spermatozoa and leucocytes on sperm functions in non-leucocytospermic patients. Fertility and Sterility 2005, 83(3):635-642.
10. Donà G., Fiore C., Tibaldi E., Frezzato F., Andrisani A., Ambrosini G., et al. Endogenous reactive oxygen species content and modulation of tyrosine phosphorylation during sperm capacitation. International Journal of Andrology 2011, 34:411-419.
11. Kim J.S., Heo K., Yi J.M., Gong E.J., Yang K., Moon C., et al. Genistein mitigates radiation-induced testicular injury. Phytotherapy Research 2011, (December). [Epub ahead of print]. 10.1002/ptr.3689.
12. Agarwal A., Deepinder F., Sharma R.K., Ranga G., Li J. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertility and Sterility 2008, 89:124-128.
13. Agarwal A., Desai N.R., Makker K., Varghese A., Mouradi R., Sabanegh E., et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertility and Sterility 2008, 92(4):1318-1325.
14. Agarwal A., Makker K., Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. American Journal of Reproductive Immunology 2008, 59:2-11.
15. Aitken R.J., Bennetts L.E., Sawyer D., Wiklendt A.M., King B.V. Impact of radio frequency electromagnetic radiation on DNA integrity in the male germline. International Journal of Andrology 2005, 28:171-179.
16. Balci M., Devrim E., Durak I. Effects of mobile phones on oxidant/antioxidant balance in cornea and lens of rats. Current Eye Research 2007, 32(1):21-25.
17. Esmekaya M.A., Ozer C., Seyhan N. 900MHz pulse-modulated radiofrequency radiation induces oxidative stress on heart, lung, testis and liver tissues. General Physiology and Biophysics 2011, 30(1):84-89.
18. Friedman J., Kraus S., Hauptman Y., Schiff Y., Seger R. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochemical Journal 2007, 405(3):559-568.
19. Meral I., Mert H., Mert N., Deger Y., Yoruk I., Yetkin A., et al. Effects of 900-MHz electromagnetic field emitted from cellular phone on brain oxidative stress and some vitamin levels of guinea pigs. Brain Research 2007, 1169:120-124.
20. Oktem F., Ozguner F., Mollaoglu H., Koyu A., Uz E. Oxidative damage in the kidney induced by 900-MHz-emitted mobile phone: protection by melatonin. Archives of Medical Research 2005, 36(4):350-355.
21. Oral B., Guney M., Ozguner F., Karahan N., Mungan T., Comlekci S., et al. Endometrial apoptosis induced by a 900-MHz mobile phone: preventive effects of vitamins E and C. Advances in Therapy 2006, 23(6):957-973.
22. Ozguner F., Bardak Y., Comlekci S. Protective effects of melatonin and caffeic acid phenethyl ester against retinal oxidative stress in long-term use of mobile phone: a comparative study. Molecular and Cellular Biochemistry 2006, 282(1-2):83-88.
23. De Iuliis G.N., Newey R.J., King B.V., Aitken R.J. Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro. PLoS One 2009, 4:e6446.
24. Erogul O., Oztas E., Yildirim I., Kir T., Aydur E., Komesli G., et al. Effects of electromagnetic radiation from a cellular phone on human sperm motility: an in vitro study. Archives of Medical Research 2006, 37:840-843.
25. Johnson R.D., Navratil M., Poe B.G., Xiong G., Olson K.J., Ahmadzadeh H., et al. Analysis of mitochondria isolated from single cells. Analytical and Bioanalytical Chemistry 2007, 387:107-118.
26. Kotnik T., Miklavcic D. Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. Biophysical Journal 2006, 90:480-491.
27. Sharma R.K., Pasqualotto F.F., Nelson D.R., Thomas A.J., Agarwal A. The reactive oxygen species - total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Human Reproduction 1999, 14:2801-2807.
28. Dasdag S., Ketani M.A., Akdag Z., Ersay A.R., Sari I., Demirtas O.C., et al. Whole-body microwave exposure emitted by cellular phones and testicular function of rats. Urological Research 1999, 27:219-223.
29. Dasdag S., Zulkuf Akdag M., Aksen F., Yilmaz F., Bashan M., Mutlu Dasdag M., et al. Whole body exposure of rats to microwaves emitted from a cell phone does not affect the testes. Bioelectromagnetics 2003, 24:182-188.
30. Irmak M.K., Fadillioglu E., Gulec M., Erdogan H., Yagmurca M., Akyol O. Effects of electromagnetic radiation from a cellular telephone on the oxidant and antioxidant levels in rabbits. Cell Biochemistry and Function 2002, 20:279-283.
31. Ribeiro E.P., Rhoden E.L., Horn M.M., Rhoden C., Lima L.P., Toniolo L. Effects of subchronic exposure to radio frequency from a conventional cellular telephone on testicular function in adult rats. Journal of Urology 2007, 177:395-399.
32. Friedman J., Kraus S., Hauptman Y., Schiff Y., Seger R. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochemical Journal 2007, 405:559-568.
33. Wdowiak A., Wdowiak L., Wiktor H. Evaluation of the effect of using mobile phones on male fertility. Annals of Agricultural and Environmental Medicine 2007, 14:169-172.
34. Dasdag S., Akdag M.Z., Ulukaya E., Uzunlar A.K., Yegin D. Mobile phone exposure does not induce apoptosis on spermatogenesis in rats. Archives of Medical Research 2008, 39(1):40-44.
35. Falzone N., Huyser C., Franken D.R., Leszczynski D. Mobile phone radiation does not induce pro-apoptosis effects in human spermatozoa. Radiation Research 2010, 174(2):169-176.
36. Zhao T.Y., Zou S.P., Knapp P.E. Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. Neuroscience Letters 2007, 412(1):34-38.
37. Shiva M., Gautam A.K., Verma Y., Shivgotra V., Doshi H., Kumar S. Association between sperm quality, oxidative stress, and seminal antioxidant activity. Clinical Biochemistry 2011, 44(4):319-324.
38. Esfandiari N., Saleh R.A., Blaut A.P., Sharma R.K., Nelson D.R., Thomas A.J., et al. Effects of temperature on sperm motion characteristics and reactive oxygen species. International Journal of Fertility and Women's Medicine 2002, 47(5):227-233.
39. Wang A.W., Zhang H., Ikemoto I., Anderson D.J., Loughlin K.R. Reactive oxygen species generation by seminal cells during cryopreservation. Urology 1997, 49(6):921-925.
40. Chatterjee S., Gagnon C. Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Molecular Reproduction and Development 2001, 59(4):451-458.
41. Mazzilli F., Rossi T., Sabatini L., Pulcinelli F.M., Rapone S., Dondero F., et al. Human sperm cryopreservation and reactive oxygen species (ROS) production. Acta Europaea Fertilitatis 1995, 26(4):145-148.
42. Marmar J.L. The pathophysiology of varicoceles in the light of current molecular and genetic information. Human Reproduction Update 2001, 7:461-472.
43. Terquem A., Dadoune J.P. Morphological findings in varicocele: an ultrastructural study of 30 bilateral testicular biopsies. International Journal of Andrology 1981, 4:515-531.
44. Kim H.H., Goldstein M. Adult varicocele. Current Opinion in Urology 2008, 18:608-612.
45. Zini A., Defreitas G., Freeman M., Hechter S., Jarvi K. Varicocele is associated with abnormal retention of cytoplasmic droplets by human spermatozoa. Fertility and Sterility 2000, 74:461-464.
46. Ollero M., Gil-Guzman E., Lopez M.C., Sharma R.K., Agarwal A., Larson K., et al. Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Human Reproduction 2001, 16:1912-1921.
47. Fischer M.A., Willis J., Zini A. Human sperm DNA integrity: correlation with sperm cytoplasmic droplets. Urology 2003, 61:207-211.
48. Saleh R.A., Agarwal A., Sharma R.K., Said T.M., Sikka S.C., Thomas A.J. Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertility and Sterility 2003, 80:1431-1436.
49. Smith R., Kaune H., Parodi D., Madariaga M., Rios R., Morales I., et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Human Reproduction 2006, 21(4):986-993.
50. Hendin B.N., Kolettis P.N., Sharma R.K., Thomas A.J., Agarwal A. Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity. Journal of Urology 1999, 161:1831-1834.
51. Cocuzza M., Athayde K.S., Agarwal A., Pagani R., Sikka S.C., Lucon A.M., et al. Impact of clinical varicocele and testis size on seminal reactive oxygen species levels in a fertile population: a prospective controlled study. Fertility and Sterility 2008, 90(4):1103-1108.
52. Wu G.J., Chang F.W., Lee S.S., Cheng Y.Y., Chen C.H., Chen I.C. Apoptosis-related phenotype of ejaculated spermatozoa in patients with varicocele. Fertility and Sterility 2009, 91:831-837.
53. Chen C.H., Lee S.S., Chen D.C., Chien H.H., Chen I.C., Chu Y.N., et al. Apoptosis and kinematics of ejaculated spermatozoa in patients with varicocele. Journal of Andrology 2004, 25:348-353.
54. Abd-Elmoaty M.A., Saleh R., Sharma R., Agarwal A. Increased levels of oxidants and reduced antioxidants in semen of infertile men with varicocele. Fertility and Sterility 2010, 94(4):1531-1534.
55. Mostafa T., Anis T., Imam H., El-Nashar A.R., Osman I.A. Seminal reactive oxygen species-antioxidant relationship in fertile males with and without varicocele. Andrologia 2009, 41:125-129.
56. Pasqualotto F.F., Sundaram A., Sharma R.K., Borges E., Pasqualotto E.B., Agarwal A. Semen quality and oxidative stress scores in fertile and infertile patients with varicocele. Fertility and Sterility 2008, 89:602-607.
57. Barbieri E.R., Hidalgo M.E., Venegas A., Smith R., Lissi E.A. Varicocele associated - decrease in antioxidant defences. Journal of Andrology 1999, 20:713-717.
58. El-Domyati M.M., Al-Din A.B.M., Barakat M.T., El-Fakahany H.M., Honig S., Xu J., et al. The expression and distribution of deoxyribonucleic acid repair and apoptosis markers in testicular germ cells of infertile varicocele patients resembles that of old fertile men. Fertility and Sterility 2010, 93:795-801.
59. Smit M., Romijn J.C., Wildhagen M.F., Veldhoven J.L., Weber R.F., Dohle G.R. Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. Journal of Urology 2010, 183:270-274.
60. Zini A., Blumenfeld A., Libman J., Willis J. Beneficial effect of microsurgical varicocelectomy on human sperm DNA integrity. Human Reproduction 2005, 20:1018-1021.
61. Nasr-Esfahani M.H., Abasi H., Razavi S., Ashrafi S., Tavalaee M. Varicocelectomy: semen parameters and protamine deficiency. International Journal of Andrology 2009, 32:115-122.
62. Haydardedeoglu B., Turunc T., Kilicdag E.B., Gul U., Bagis T. The effect of prior varicocelectomy in patients with nonobstructive azoospermia on intracytoplasmic sperm injection outcomes: a retrospective pilot study. Urology 2010, 75:83-86.
63. Ficarra V., Cerruto M.A., Liguori G., Mazzoni G., Minucci S., Tracia A., et al. Treatment of varicocele in subfertile men: the Cochrane Review - a contrary opinion. European Urology 2006, 49:258-263.
64. Narayana K., Al-Bader M., Mousa A., Khan K.M. Molecular effects of chemotherapeutic drugs and their modulation by antioxidants in the testis. European Journal of Pharmacology 2012, 674(2-3):207-216.
65. Farombi E.O., Ugwuezunmba M.C., Ezenwadu T.T., Ovevemi M.O., Ekor M. Tetracycline-induced reproductive toxicity in male rats: effects of vitamin C and N-acetylcysteine. Experimental and Toxicologic Pathology 2008, 60(1):77-85.
66. Naravana K. An aminoglycoside antibiotic gentamycin induces oxidative stress, reduces antioxidant reserve and impairs spermatogenesis in rats. Journal of Toxicological Sciences 2008, 33(1):85-96.
67. Ovagbemi A.A., Adedara I.A., Saba A.B., Farombi E.O. Role of oxidative stress in reproductive toxicity induced by co-administration of chloramphenicol and multivitamin-haematinics complex in rats. Basic & Clinical Pharmacology & Toxicology 2010, 107(3):703-708.
68. Adedara I.A., Farombi E.O. Induction of oxidative damage in the testes and spermatozoa and hematotoxicity in rats exposed to multiple doses of ethylene glycol monoethyl ether. Human and Experimental Toxicology 2010, 29(10):801-812.
69. Chitra K.C., Latchoumycandane C., Mathur P.P. Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology 2003, 185(1-2):119-127.
70. Chitra K.C., Latchoumycandane C., Mathur P.P. Induction of oxidative stress in rat epididymal sperm after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Archives of Toxicology 2002, 76(2):113-118.
71. Pant N., Shukla M., Kumar Patel D., Shukla Y., Mathur N., Kumar Gupta Y., et al. Correlation of phthalate exposures with semen quality. Toxicology and Applied Pharmacology 2008, 231(1):112-116.
72. Ong C.N., Shen H.M., Chia S.E. Biomarkers for Male Reproductive Health hazards: are they available?. Toxicology Letters 2002, 134:17-30.
73. Telisman S., Cvitkovic P., Jurasovic J., Pizent A., Gavella M., Rocić B. Semen quality and reproductive endrocrine function in relation to biomarkers of lead, cadmium, zinc and copper in men. Environmental Health Perspectives 2000, 108:45-53.
74. 2 exposure on human sperm motility parameters, reactive oxygen species levels and nitric oxide levels. Andrologia 2010, 42:206-210.
75. Marchlewicz M., Michalska T., Wiszniewska B. Detection of lead-induced oxidative stress in the rat epididymis by chemiluminescence. Chemosphere 2004, 57(10):1553-1562.
76. Kiziler A.R., Aydemir B., Onaran I., Alici B., Ozkara H., Gulyasar T., et al. High levels of cadmium and lead in seminal fluid and blood of smoking men are associated with high oxidative stress and damage in infertile subjects. Biological Trace Element Research 2007, 120(1-3):82-91.
77. Zenzes M.T. Smoking and reproduction: gene damage to human gametes and embryos. Human Reproduction Update 2000, 6:122-131.
78. Pasupathi P., Saravanan G., Farook J. Oxidative stress biomarkers and antioxidant status in cigarette smokers compared to nonsmokers. Journal of Pharmaceutical Sciences & Research 2009, 1:55-62.
79. Gornig V.M., Schirren C. Effect of exogenous toxins on fertility. Fortschritte der Medizin 1996, 114(14):169-171.
80. Keck C., Bramkamp G., Behre H.M., Muller C., Jockenhovel F., Nieschlag E. Lack of correlation between cadmium in seminal plasma and fertility status of nonexposed individuals and two cadmium-exposed patients. Reproductive Toxicology 1995, 9(1):35-40.
81. Pacifici R., Altieri I., Gandini L., Lenzi A., Passa A.R., Pichini S., et al. Environmental tobacco smoke: nicotine and cotinine concentration in semen. Environmental Research 1995, 68(1):69-72.
82. Pacifici R., Altieri I., Gandini L., Lenzi A., Pichini S., Rosa M., et al. Nicotine, cotinine and trans-3-hydroxycotinine levels in seminal plasma of smokers: effects on sperm parameters. Therapeutic Drug Monitoring 1993, 15(5):358-363.
83. Saaranen M., Kantola M., Saarikoski S., Vanha Perttula T. Human seminal plasma cadmium: comparison with fertility and smoking habits. Andrologia 1989, 21(2):140-145.
84. Zenzes M.T., Bielecki R., Reed T.E. Detection of benzo(a)pyrene diolepoxide-DNA adducts in sperm of men exposed to cigarette smoke. Fertility and Sterility 1999, 72(2):330-335.
85. Fraga C.G., Motchnik P.A., Wyrobek A.J., Rempel D.M., Ames B.N. Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutation Research 1996, 351:199-203.
86. Hammadeh M.E., Hamad M.F., Montenarh M., Fischer-Hammadeh C. Protamine contents and P1/P2 ratio in human spermatozoa from smokers and non-smokers. Human Reproduction 2010, 25(11):2708-2720.
87. Saleh R.A., Agarwal A., Sharma R.K., Nelson D.R., Thomas A.J. Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study. Fertility and Sterility 2002, 78:491-499.
88. Mostafa T., Tawadrous G., Roaia M.M.F., Amer M.K., Kader R.A., Aziz A. Effect of smoking on seminal plasma ascorbic acid in infertile and fertile males. Andrologia 2006, 38:221-224.
89. Pasqualotto F.F., Umezu F.M., Salvador M., Borges E., Sobreiro B.P., Pasqualotto E.B. Effect of cigarette smoking on antioxidant levels and presence of leucocytospermia in infertile men: a prospective study. Fertility and Sterility 2008, 90:278-283.
90. Colagar A.H., Marzony E.T., Chaichi M.J. Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutrition Research 2009, 29(2):82-88.
91. Liu R.Z., Gao J.C., Zhang H.G., Wang R.X., Zhang Z.H., Liu X.Y. Seminal plasma zinc level may be associated with the effect of cigarette smoking on sperm parameters. Journal of International Medical Research 2010, 38(3):923-928.
92. Pryor W.A., Hales B.J., Premovic P.I., Church D.F. The radicals in cigarette tar: their nature and suggested physiological implications. Science 1983, 220:425-427.
93. Pryor W.A., Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Annals of the New York Academy of Sciences 1993, 868:12-27.
94. Agarwal A., Prabakaran S.A., Said T.M. Prevention of oxidative stress injury to sperm. Journal of Andrology 2005, 26:654-660.
95. Elshal M.F., El-Sayed I.H., Elsaied M.A., El-Masry S.A., Kumosani T.A. Sperm head defects and disturbances in spermatozoal chromatin and DNA integrities in idiopathic infertile subjects: association with cigarette smoking. Clinical Biochemistry 2009, 42(7-8):589-594.
96. Linschooten J.O., Laubenthal J., Cemeli E., Baumgartner A., Anderson D., Sipinen V.E., et al. Incomplete protection of genetic integrity of mature spermatozoa against oxidative stress. Reproductive Toxicology 2011, 32(1):106-111.
97. Sepaniak S., Forges T., Fontaine B., Gerard H., Foliguet B., Guillet May F., et al. Negative impact of cigarette smoking on male fertility: from spermatozoa to the offspring. Journal de Gynecologie, Obstetrique et Biologie de la Reproduction 2004, 33(5):384-390.
98. Sepaniak S., Forges T., Gerard H., Foliguet B., Bene M.C., Monnier-Barbarino P. The influence of cigarette smoking on human sperm quality and DNA fragmentation. Toxicology 2006, 223(1-2):54-60.
99. Aoki V.W., Emery B.R., Liu L., Griffin J., Carrell D.T. Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. Journal of Andrology 2006, 27:890-898.
100. Aoki V.W., Liu L., Jones K.P., Hatasaka H.H., Gibson M., Peterson C.M., et al. Sperm protamine 1/protami2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertility and Sterility 2006, 86:1408-1415.
101. Oliva R. Protamines and male infertility. Human Reproduction Update 2006, 12:417-435.
102. Gaur D.S., Talekar M., Pathak V.P. Effect of cigarette smoking on semen quality of infertile men. Singapore Medical Journal 2007, 48(2):119-123.
103. Hassa H., Yildirim A., Can C., Turgut M., Tanir H.M., Senses T., et al. Effect of smoking on semen parameters of men attending an infertility clinic. Clinical and Experimental Obstetrics and Gynecology 2006, 33(1):19-22.
104. Ramlau Hansen C.H., Thulstrup A.M., Aggerholm A.S., Jensen M.S., Toft G., Bonde J.P. Is smoking a risk factor for decreased semen quality? A cross-sectional analysis. Human Reproduction 2007, 22(1):188-196.
105. Amaral S., Oliveira P.J., Ramalho-Santos J. Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Current Diabetes Reviews 2008, 4(1):46-54.
106. Shrilatha B., Muralidhara H.B. Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences. Reproductive Toxicology 2007, 23(4):578-587.
107. Aitken R.J., De Iuliis G.N. Origins and consequences of DNA damage in male germ cells. Reproductive Biomedicine Online 2007, 14:727-733.
108. Tremellen K. Oxidative stress and male infertility - a clinical perspective. Human Reproduction Update 2008, 14(3):243-258.
109. Padron O.F., Brackett N.L., Sharma R.K., Lynne C.M., Thomas A.J., Agarwal A. Seminal reactive oxygen species and sperm motility and morphology in men with spinal cord injury. Fertility and Sterility 1997, 67(6):1115-1120.
110. Brackett N.L., Ibrahim E., Grotas J.A., Aballa T.C., Lynne C.M. Higher sperm DNA damage in semen from men with spinal cord injuries compared to controls. Journal of Andrology 2008, 29:93-99.
111. La Vignera S., Condorelli R.A., Vicari E., D'Agata R., Calogero A.E. Sperm DNA damage in patients with chronic viral C hepatitis. European Journal of Internal Medicine 2012, 23(1):e19-e24.
112. La Vignera S., Calogero A.E., Cannizzaro M.A., Vicari E. Mono or bilateral inflammatory postmicrobial prostato-vesciculo-epididymitis: differences in semen parameters and reactive oxygen species production. Minerva Endocrinologica 2006, 31(4):263-272.
113. Vicari E., La Vignera S., Castiglione R., Calogero A.E. Sperm parameter abnormalities, low seminal fructose and reactive oxygen species overproduction do not discriminate patients with unilateral or bilateral post-infectious inflammatory prostato-vesiculo-epididymitis. Journal of Endocrinological Investigation 2006, 29(1):18-25.
114. Potts J.M., Pasqualotto F.F. Seminal oxidative stress in patients with chronic prostatitis. Andrologia 2003, 35(5):304-308.
115. Shahed A.R., Shoskes D.A. Oxidative stress in prostatic fluid of patients with chronic pelvic pain syndrome: correlation with gram positive bacterial growth and treatment response. Journal of Andrology 2000, 21(5):669-675.
116. Vicari E. Effectiveness and limits of antimicrobial treatment on seminal leucocyte concentration and related reactive oxygen species production in patients with male accessory gland infection. Human Reproduction 2000, 15(12):2536-2544.
117. Henkel R., Maass G., Hajimohammad M., Menkveld R., Stalf T., Villegas J., et al. Urogenital inflammation: changes of leucocytes and ROS. Andrologia 2003, 35(5):309-313.
118. Vicari E. Seminal leucocyte concentration and related specific reactive oxygen species production in patients with male accessory gland infections. Human Reproduction 1999, 14(8):2025-2030.
119. Ochsendorf F.R. Infections in the male genital tract and reactive oxygen species. Human Reproduction Update 1999, 5(5):399-420.
120. Wang A., Fanning L., Anderson D.J., Loughlin K.R. Generation of reactive oxygen species by leucocytes and sperm following exposure to urogenital tract infection. Archives of Andrology 1997, 39(1):11-17.
121. Potts J.M., Sharma R., Pasqualotto F., Nelson D., Hall G., Agarwal A. Association of ureaplasma urealyticum with abnormal reactive oxygen species levels and absence of leucocytospermia. Journal of Urology 2000, 163(6):1775-1778.
122. Paavonen J., Eggert-Kruse W. Chlamydia trachomatis: impact on human reproduction. Human Reproduction Update 1999, 5:433-447.
123. World Health Organization Global prevalence and incidence of selected curable sexually transmitted infections: overview and estimates 2001, World Health Organization, Geneva, p. 1-43.
124. Bollmann R., Engel S., Petzoldt R., Göbel U.B. Chlamydia trachomatis in andrologic patients - direct and indirect detection. Infection 2001, 29(3):113-118.
125. Urata K., Narahara H., Tanaka Y., Egashira T., Takayama F., Miyakawa I. Effect of endotoxin-induced reactive oxygen species on sperm motility. Fertility and Sterility 2001, 76(1):163-166.
126. Fraczek M., Kurpisz M. Inflammatory mediators exert toxic effects of oxidative stress on human spermatozoa. Journal of Andrology 2007, 28(2):325-333.
127. Agarwal A., Nalella K.P., Allamaneni S.S., Said T.M. Role of antioxidants in treatment of male infertility: an overview of the literature. Reproductive Biomedicine Online 2004, 8:616-627.
128. Angelopoulou R., Kyriazoglou M. Sperm oxidative damage and the role of ROS in male infertility. Archives of Hellenic Medicine 2005, 22:443-446.
129. Weir C.P., Robaire B. Spermatozoa have decreased antioxidant enzymatic capacity and increased ROS production during aging in the Brown Norway Rat. Journal of Andrology 2007, 28:229-240.