Book contents
- Infertility in the Male
- Infertility in the Male
- Copyright page
- Contents
- Contributors
- Foreword
- Abbreviations
- Introduction
- Section 1 Scientific Foundations of Male Infertility
- Section 2 Clinical Evaluation of the Infertile Male
- Section 3 Laboratory Diagnosis of Male Infertility
- Chapter 17 Laboratory Evaluation of the Infertile Male
- Chapter 18 Advanced Diagnostic Approaches to Male Infertility
- Chapter 19 Evaluating Defects in Sperm Function
- Chapter 20 Cryopreservation of Sperm – History and Current Practice
- Section 4 Treatment of Male Infertility
- Section 5 Health Care Systems and Culture
- Index
- References
Chapter 19 - Evaluating Defects in Sperm Function
from Section 3 - Laboratory Diagnosis of Male Infertility
Published online by Cambridge University Press: 08 July 2023
Book contents
- Infertility in the Male
- Infertility in the Male
- Copyright page
- Contents
- Contributors
- Foreword
- Abbreviations
- Introduction
- Section 1 Scientific Foundations of Male Infertility
- Section 2 Clinical Evaluation of the Infertile Male
- Section 3 Laboratory Diagnosis of Male Infertility
- Chapter 17 Laboratory Evaluation of the Infertile Male
- Chapter 18 Advanced Diagnostic Approaches to Male Infertility
- Chapter 19 Evaluating Defects in Sperm Function
- Chapter 20 Cryopreservation of Sperm – History and Current Practice
- Section 4 Treatment of Male Infertility
- Section 5 Health Care Systems and Culture
- Index
- References
Summary
Semen analysis has been the standard of clinical laboratory assessment(s) of male fertility potential for more than 70 years [1–4]. Methodologies for performing the semen analysis, along with standard practices to ensure quality in clinical laboratory practices throughout testing, have been codified in multiple World Health Organization publications [5–9]. A common, and albeit disappointing, conclusion regarding the semen analysis is that the lower reference limits have limited predictive value for fertility or, for that matter, infertility (see, for example, [10–14]). A partial explanation for this inadequacy is that, with the exception of sperm motility, sperm function requirements that are necessary for successful fertilization and term delivery are not assessed in the semen analysis. This dilemma impacts the ability of clinicians to provide an evident diagnosis to the patient couple concerning the presence/absence of male subfertility, especially in the absence of genetic, hormonal, or urogenital abnormalities. This dilemma becomes further exacerbated for the clinician who must decide on an appropriate therapeutic strategy to address the infertility and for the patients who balance their desires in conjunction with spiritual, emotional, and financial considerations.
- Type
- Chapter
- Information
- Infertility in the Male , pp. 363 - 380Publisher: Cambridge University PressPrint publication year: 2023
References
MacLeod, J. The male factor in fertility and infertility; an analysis of ejaculate volume in 800 fertile men and in 600 men in infertile marriage. Fertil Steril 1950;1:347–61.Google Scholar
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. II. Spermatozoon counts in 1000 men of known fertility and in 1000 cases of infertile marriage. J Urol 1951;66:436–49.Google Scholar
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. III. An analysis of motile activity in the spermatozoa of 1000 fertile men and 1000 men in infertile marriage. Fertil Steril 1951;2:187–204.Google Scholar
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. IV. Sperm morphology in fertile and infertile marriage. Fertil Steril 1951;2:394–414.CrossRefGoogle ScholarPubMed
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 1st ed. Singapore: Press Concern, 1980.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction. 2nd ed. Cambridge: Cambridge University Press, 1987.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 3rd ed. Cambridge: Cambridge University Press, 1992.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th ed. Cambridge: Cambridge University Press, 1999.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th ed. Geneva: World Health Organization, 2010.Google Scholar
Amann, RP. Can the fertility potential of a seminal sample be predicted accurately? J Androl 1989;10:89.Google Scholar
Smith, KD, Rodriguez-Rigau, LJ, Steinberger, E. Relation between indices of semen analysis and pregnancy rate in infertile couples. Fertil Steril 1977;28:1314–19.CrossRefGoogle ScholarPubMed
Guzick, DS, Overstreet, JW, Factor-Litvak, P, et al. Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med 2001;345:1388–93.Google Scholar
Patel, AS, Leong, JY, Ramasamy, R. Prediction of male infertility by the World Health Organization laboratory manual for assessment of semen analysis: a systematic review. Arab J Urol 2018;16:96–102.Google Scholar
Blasco, L. Clinical tests of sperm fertilizing ability. Fertil Steril 1984;41:177–92.Google ScholarPubMed
Liu, DY, Baker, HWG. Tests of human sperm function and fertilization in vitro. Fertil Steril 1992;58:465–83.Google Scholar
Muller, CH. Rationale, interpretation, validation, and uses of sperm function tests. J Androl 2000;21:10–30.Google Scholar
Lamb, DJ. Semen analysis in 21st century medicine: the need for sperm function testing. Asian J Androl 2010;12:64–70.Google Scholar
De Jonge, C. Semen analysis: looking for an upgrade in class. Fertil Steril 2012;97:260–6.CrossRefGoogle ScholarPubMed
Oehninger, S, Franken, DR, Ombelet, W. Sperm functional tests. Fertil Steril 2014;102:1528–33.Google Scholar
Mortimer, D. The functional anatomy of the human spermatozoon: relating ultrastructure and function. Mol Human Reprod 2018;24:567–92.Google Scholar
Kricka, LJ, Wilding, P. Evolution of sperm testing – a bright future? Clin Chem 2019;65:212–14.CrossRefGoogle ScholarPubMed
Mortimer, ST. A critical review of the physiological importance and analysis of sperm movement in mammals. Hum Reprod Update 1997;3:403–39.Google Scholar
De Jonge, C. Biological basis for human capacitation. Hum Reprod Update 2005;11:205–14.Google Scholar
Austin, CR. Observations on the penetration of sperm into the mammalian egg. Aust J Sci Res 1951;4(series B):581–96.Google Scholar
Chang, MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951;168:697–8.CrossRefGoogle ScholarPubMed
De Jonge, C. Biological basis for human capacitation – revisted. Hum Reprod Update 2017;23:289–99.Google Scholar
Gervasi, MG, Visconti, PE. Chang’s meaning of capacitation: a molecular perspective. Mol Reprod Dev 2016;83:860–74.Google Scholar
Jin, SK, Yand, WX. Factors and pathways involved in capacitation: how are they regulated? Oncotarget 2017;8:3600–27.Google Scholar
Puga Molina, LC, Luque, GM, Balestrini, PA, Marín-Briggiler, CI, Romarowski, A, Buffone, MG. Molecular basis of human sperm capacitation. Front Cell Dev Biol 2018;6:72.Google Scholar
Aitken, RJ. Reactive oxygen species as mediators of sperm capacitation and pathological damage. Mol Reprod Dev 2017;84:1039–52.Google Scholar
Henkel, R, Samanta, L, Agarwal, A (eds). Oxidants, Antioxidants, and Impact of the Oxidative Status in Male Reproduction. London: Elsevier, 2019.Google Scholar
Rubenstein, BB, Strauss, H, Lazarus, ML, Hankin, H. Sperm survival in women: motile sperm in fundus and tubes of surgical cases. Fertil Steril 1951;2:15–19.Google Scholar
Settlage, DS, Motoshima, M, Tredway, DR. Sperm transport from the external cervical os to the fallopian tubes in women: a time and quantitation study. Fertil Steril 1973;24:655–61.Google Scholar
Ahlgren, M. Sperm transport to and survival in the human fallopian tube. Gynecol Invest 1975;6:206–14.Google Scholar
Yanagimachi, R. The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil 1970;23:193–6.Google Scholar
Oei, SG. The postcoital test: a controversial investigation. Eur J Obstet Gynecol 1998;77:123–4.Google Scholar
Ola, B, Afnan, M, Papaioannou, S, Sharif, K, Bjorndahl, L, Coomarasamy, A. Accuracy of sperm-cervical mucus penetration tests in evaluating sperm motility in semen: a systematic quantitative review. Hum Reprod 2003;18:1037–46.Google Scholar
Kesseru, E. In vivo sperm penetration and in vitro sperm migration tests. Fertil Steril 1973;24:584–91.Google Scholar
Alexander, NJ. Evaluation of male infertility with an in vitro cervical mucus penetration test. Fertil Steril 1981;36:201–8.Google Scholar
Mortimer, D, Mortimer, ST, Shu, MA, Swart, R. A simplified approach to sperm-cervical mucus interaction testing using a hyaluronate migration test. Hum Reprod 1990;5:835–41.CrossRefGoogle ScholarPubMed
Ivic, A, Onyeaka, H, Girling, A, et al. Critical evaluation of methylcellulose as an alternative medium in sperm migration tests. Hum Reprod 2002;17:143–9.Google Scholar
David, MP, Amit, A, Bergman, A, Yedwab, G, Paz, GF, Hommonai, ZT. Sperm penetration in vitro: correlations between parameters of sperm quality and the penetration capacity. Fertil Steril 1979;32:676–80.CrossRefGoogle Scholar
Katz, DF, Overstreet, JW, Hanson, FW. A new quantitative test for sperm penetration into cervical mucus. Fertil Steril 1980;33:179–86.Google Scholar
Overstreet, JW, Coats, C, Katz, DF, Hanson, FW. The importance of seminal plasma for sperm penetration of cervical mucus. Fertil Steril 1980;34:569–72.CrossRefGoogle ScholarPubMed
Makler, A. A new multiple exposure photography method for objective human spermatozoal motility determination. Fertil Steril 1978;30:192–9.Google Scholar
Overstreet, JW, Katz, DF, Hanson, FW, Fonseca, JR. A simple inexpensive method for objective assessment of human sperm movement characteristics. Fertil Steril 1979;31:162–72.Google Scholar
Katz, DF, Overstreet, JW, Hanson, FW. Variations within and amongst normal men of movement characteristics of seminal spermatozoa. J Reprod Fertil 1981;62:221–8.Google Scholar
Aitken, RJ, Best, FSM, Richardson, DW, et al. An analysis of sperm function in cases of unexplained infertility: conventional criteria, movement characteristics, and fertilizing capacity. Fertil Steril 1982;38:212–21.CrossRefGoogle ScholarPubMed
Katz, DF, Overstreet, JW. Sperm motility assessment by videomicrography. Fertil Steril 1981;35:188–93.CrossRefGoogle ScholarPubMed
Mathur, S, Carlton, M, Ziegler, J, Rust, PF, Williamson, HO. A computerized sperm motion analysis. Fertil Steril 1986;46:484–8.CrossRefGoogle ScholarPubMed
Holt, WV, Moore, HDM, Hillier, SG. Computer-assisted measurement of sperm swimming speed in human semen: correlation of results with in vitro fertilization assays. Fertil Steril 1985;44:112–19.Google Scholar
Barratt, CLR, Tomlinson, MJ, Cooke, ID. Prognostic significance of computerized motility analysis for in vivo fertility. Fertil Steril 1993;60:520–5.Google Scholar
Irvine, DS, Macleod, IC, Templeton, AA, Masterton, A, Taylor, A. A prospective clinical study of the relationship between the computer-assisted assessment of human semen quality and the achievement of pregnancy in vivo. Hum Reprod 1994;9:2324–34.Google Scholar
Macleod, IC, Irvine, DS. The predictive value of computerized-assisted semen analysis in the context of a donor insemination programme. Hum Reprod 1995;10:580–6.Google Scholar
Larsen, L, Scheike, T, Jensen, TK, et al.; The Danish First Pregnancy Planner Study Team. Computer-assisted semen analysis parameters as predictors for fertility of men from the general population. Hum Reprod 2000;15:1562–7.Google Scholar
Burke, RK, Kapinos, LJ. The effect of in vitro capacitation on sperm velocity and motility as measured by an in-office, integrated, microcomputerized system for semen analysis. Int J Fertil 1985;30:10–17.Google Scholar
Kay, VJ, Robertson, L. Hyperactivated motility of human spermatozoa: a review of physiological function and application in assisted reproduction. Hum Reprod Update 1998;776–86.Google Scholar
Mortimer, ST, van der Horst, G, Mortimer, D. The future of computer-aided sperm analysis. Asian J Androl 2015;17:545–53.Google Scholar
Mortimer, ST, De Jonge, CJ. CASA—Computer-aided sperm analysis. In: Skinner, MK, ed. Encyclopedia of Reproduction, 2nd ed, Vol. 5. Boston, MA: Academic Press, Elsevier, 2018; pp. 59–63. Available from: dx.doi.org/10.1016/B978-0-12-801238-3.64935-8.Google Scholar
Wang, C, Lee, GS, Leung, A, Surrey, ES, Chan, SY. Human sperm hyperactivation and acrosome reaction and their relationships to human in vitro fertilization. Fertil Steril 1993;59:1221–7.CrossRefGoogle ScholarPubMed
Sukcharoen, N, Keith, J, Irvine, DS, Aitken, RJ. Definition of the optimal criteria for identifying hyperactivated human spermatozoa at 25 Hz using in-vitro fertilization as a functional end-point. Hum Reprod 1995;10:2928–37.CrossRefGoogle ScholarPubMed
Wang, C, Leung, A, Tsoi, W-L, et al. Evaluation of human sperm hyperactivated motility and its relationship with the zona-free hamster oocyte sperm penetration assay. J Androl 1991;12:253–7.Google Scholar
Macleod, IC, Irvine, DS, Masterton, A, Taylor, A, Templeton, AA. Assessment of the conventional criteria of semen quality by computer-assisted image analysis: evaluation of the Hamilton-Thorn motility analyser in the context of a service andrology laboratory. Hum Reprod 1994;9:310–19.Google Scholar
ESHRE Andrology Special Interest Group. Consensus workshop on advanced diagnostic andrology techniques. Hum Reprod 1996;11:1463–79.Google Scholar
Yanagimachi, R. In vitro acrosome reaction and capacitation of golden hamster spermatozoa by bovine follicular fluid and its fractions. J Exp Zool 1969;170:269–80.Google Scholar
Bavister, BD. Environmental factors important for in vitro fertilization in the hamster. J Reprod Fertil 1969;18:S544–5.Google Scholar
Edwards, RG, Steptoe, PC, Purdy, JM. Fertilization and cleavage in vitro of preovulatory human oocytes. Nature 1970;227:1307–9.Google Scholar
Yanagimachi, R, Yanagimachi, H, Rogers, BJ. The use of zona-free animal ova as a test-system for the assessment of the fertilizing capacity of Human spermatozoa. Biol Reprod 1976;15:471–6.Google Scholar
Overstreet, JW, Hembree, WC. Penetration of the zona pellucida of nonliving human oocytes by human spermatozoa in vitro. Fertil Steril 1976;27:815–31.CrossRefGoogle ScholarPubMed
Rogers, BJ. The sperm penetration assay: its usefulness reevaluated. Fertil Steril 1985;43:821–40.Google Scholar
Yanagimachi, R, Lopata, A, Odom, CB, Bronson, RA, Mahi, CA, Nicolson, GL. Retention of biologic characteristics of zona pellucida in highly concentrated salt solution: the use of salt-stored eggs for assessing the fertilizing capacity of spermatozoa. Fertil Steril 1979;31:562–74.CrossRefGoogle ScholarPubMed
Burkman, LJ, Coddington, CC, Franken, DR, Krugen, TF, Rosenwaks, Z, Hogen, GD. The hemizona assay (HZA): development of a diagnostic test for the binding of human spermatozoa to the human hemizona pellucida to predict fertilization potential. Fertil Steril 1988;49:688–97.Google Scholar
Franken, DR, Burkman, LJ, Oehninger, SC, et al. Hemizona assay using salt-stored human oocytes: evaluation of zona pellucida capacity for binding human spermatozoa. Gamete Res 1989;22:15–26.Google Scholar
Franken, DR, Oosthuizen, WT, Cooper, S, et al. Electron microscopic evidence on the acrosomal status of bound sperm and their penetration into human hemizonae pellucida after storage in a buffered salt solution. Andrologia 1991;23:205–8.Google Scholar
Franken, DR, Windt, ML, Kruger, TF, Oehninger, S, Hodgen, GD. Comparison of sperm binding potential of uninseminated, inseminated-unfertilized, and fertilized-noncleaved human oocytes under hemizona assay conditions. Mol Reprod Dev 1991;30:56–61.Google Scholar
Franken, DR, Coddington, CC, Burkman, LJ, et al. Defining the valid hemizona assay: accounting for binding variability within zonae pellucidae and within semen samples from fertile males. Fertil Steril 1991;56:1156–61.Google Scholar
Oehninger, S, Mahony, M, Ozgür, K, Kolm, P, Kruger, T, Franken, D. Clinical significance of human sperm-zona pellucida binding. Fertil Steril 1997;67:1121–7.CrossRefGoogle ScholarPubMed
Liu, DY, Lopata, A, Johnston, WI, Baker, HW. A human sperm-zona pellucida binding test using oocytes that failed to fertilize in vitro. Fertil Steril 1988;50:782–8.Google Scholar
Liu, DY, Clarke, GN, Lopata, A, Johnston, WI, Baker, HW. A sperm–zona pellucida binding test and in vitro fertilization. Fertil Steril 1989;52:281–7.Google Scholar
Liu, DY, Baker, HW. A new test for the assessment of sperm-zona pellucida penetration: relationship with results of other sperm tests and fertilization in vitro. Hum Reprod 1994;9:489–96.Google Scholar
Liu, DY, Baker, HW. Defective sperm-zona pellucida interaction: a major cause of failure of fertilization in clinical in-vitro fertilization. Hum Reprod 2000;15:702–8.Google Scholar
Sosa, CM, Pavarotti, MA, Zanetti, MN, Zoppino, FC, De Blas, GA, Mayorga, LS. Kinetics of human sperm acrosomal exocytosis. Mol Hum Reprod 2015;21:244–54.Google Scholar
De Jonge, CJ, Barratt, CL. Methods for the assessment of sperm capacitation and acrosome reaction excluding the sperm penetration assay. Methods Mol Biol 2013;927:113–18.Google Scholar
Overstreet, JW, Yanagimachi, R, Katz, DF, Hayashi, K, Hanson, FW. Penetration of human spermatozoa into the human zona pellucida and the zona-free hamster egg: a study of fertile donors and infertile patients. Fertil Steril 1980;33:534–42.Google Scholar
Aitken, RJ, Ross, A, Hargreave, T, Richardson, D, Best, F. Analysis of human sperm function following exposure to the ionophore A23187. Comparison of normospermic and oligozoospermic men. J Androl 1984;5:321–9.Google Scholar
De Jonge, CJ, Mack, SR, Zaneveld, LJD. Synchronous assay for human sperm capacitation and the acrosome reaction. J Androl 1989;10:232–9.Google Scholar
Cummins, JM, Pember, SM, Jequier, AM, Yovich, JL, Hartmann, PE. A test of the human sperm acrosome reaction following ionophore challenge. Relationship to fertility and other seminal parameters. J Androl 1991;12:98–103.Google Scholar
Aitken, RJ, Thatcher, S, Glasier, AF, Clarkson, JS, Wu, FC, Baird, DT. Relative ability of modified versions of the hamster oocyte penetration test, incorporating hyperosmotic medium or the ionophore A23187, to predict IVF outcome. Hum Reprod 1987;2:227–31.Google Scholar
Pampiglione, JS, Tan, SL, Campbell, S.The use of the stimulated acrosome reaction test as a test of fertilizing ability in human spermatozoa. Fertil Steril 1993;59:1280–4.Google Scholar
Makkar, G, Ng, EHY, Yeung, WSBY, Ho, PK. The significance of the ionophore-challenged acrosome reaction in the prediction of successful outcome of controlled ovarian stimulation and intrauterine insemination. Hum Reprod 2003;18:534–9.Google Scholar
Katsuki, T, Hara, T, Ueda, K, Tanaka, J, Ohama, K. Prediction of outcomes of assisted reproduction treatment using calcium ionophore-induced acrosome reaction. Hum Reprod 2005;20:469–75.CrossRefGoogle ScholarPubMed
Krausz, C, Bonaccorsi, L, Luconi, M, et al. Intracellular calcium increase and acrosome reaction in response to progesterone in human spermatozoa are correlated with in-vitro fertilization. Hum Reprod 1995;10:120–4.Google Scholar
Krausz, C, Bonaccorsi, L, Maggio, P, et al. Two functional assays of sperm responsiveness to progesterone and their predictive values in in-vitro fertilization. Hum Reprod 1996;11:1661–7.Google Scholar
Cross, NL, Morales, P, Overstreet, JW, Hanson, FW. Induction of acrosome reactions by the human zona pellucida. Biol Reprod 1988;38:235–44.Google Scholar
Bielfeld, P, Faridi, A, Zaneveld, LJ, De Jonge, CJ. The zona pellucida-induced acrosome reaction of human spermatozoa is mediated by protein kinases. Fertil Steril 1994;61:536–41.Google Scholar
Franken, DR, Bastiaan, HS, Oehninger, SC. Physiological induction of the acrosome reaction in human sperm: validation of a microassay using minimal volumes of solubilized, homologous zona pellucida. J Assist Reprod Genet 2000;17:374–8.Google Scholar
Franken, DR, Bastiaan, HS, Kidson, A, Wranz, P, Habenicht, UF. Zona pellucida mediated acrosome reaction and sperm morphology. Andrologia 1997;29:311–17.Google Scholar
De Jonge, CJ. The diagnostic significance of the induced acrosome reaction. Reprod Med Rev 1994;3:159–78.Google Scholar
Buttke, DE, Nelson, JL, Schlegel, PN, Hunnicutt, GR, Travis, AJ. Visualization of GM1 with cholera toxin B in live epididymal versus ejaculated bull, mouse, and human spermatozoa. Biol Reprod 2006;74:889–95.Google Scholar
Selvaraj, V, Asano, A, Buttke, DE, Sengupta, P, Weiss, RS, Travis, AJ. Mechanisms underlying the micron-scale segregation of sterols and GM1 in live mammalian sperm. J Cell Physiol 2009;218:522–36.Google Scholar
Moody, MA, Cardona, C, Simpson, AJ, Smith, TT, Travis, AJ, Ostermeier, GC. Validation of a laboratory-developed test of human sperm capacitation. Mol Reprod Dev 2017;84:408–22.Google Scholar
Cardona, C, Neri, QV, Simpson, AJ, et al. Localization patterns of the ganglioside GM1 in human sperm are indicative of male fertility and independent of traditional semen measures. Mol Reprod Dev 2017;84:423–35.Google Scholar
Babigumira, JB, Sharara, FI, Garrison, LP Jr. Projecting the potential impact of the Cap-Score™ on clinical pregnancy, live births, and medical costs in couples with unexplained infertility. J Assist Reprod Genet 2018;35:99–106.Google Scholar
Schinfeld, J, Sharara, F, Morris, R, et al. Cap-Score™ prospectively predicts probability of pregnancy. Mol Reprod Dev 2018;85:654–64.CrossRefGoogle ScholarPubMed
Kovalski, NN, de Lamirande, E, Gagnon, C. Reactive oxygen species generated by human neutrophils inhibit sperm motility: protective effect of seminal plasma and scavengers. Fertil Steril 1992;58:809–16.Google Scholar
Aitken, RJ, Clarkson, JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fert 1987;81:459–69.Google Scholar
Aitken, RJ, Clarkson, JS, Fishel, S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 1989;41:183–97.Google Scholar
Aitken, J, Krausz, C, Buckingham, D. Relationships between biochemical markers for residual sperm cytoplasm, reactive oxygen species generation, and the presence of leukocytes and precursor germ cells in human sperm suspensions. Mol Reprod Dev 1994;39:268–79.Google Scholar
de Lamirande, E, Gagnon, C. A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int J Androl 1993;16:21–5.Google Scholar
Aitken, RJ, Gordon, E, Harkiss, D, et al. Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 1998;59:1037–46.Google Scholar
Tremellen, K. Oxidative stress and male infertility – a clinical perspective. Hum Reprod Update 2008;14:243–58.Google Scholar
Aitken, RJ, Smith, TB, Jobling, MS, Baker, MA, De Iuliis, GN. Oxidative stress and male reproductive health. Asian J Androl 2014;16:31–8.Google Scholar
Aitken, RJ, Gibb, Z, Baker, MA, Drevet, J, Gharagozloo, P. Causes and consequences of oxidative stress in spermatozoa. Reprod Fertil Devel 2016;28:1–10.Google Scholar
Agarwal, A, Majzoub, A. Laboratory tests for oxidative stress. Indian J Urol 2017;33:199–206.Google Scholar
Wagner, H, Cheng, JW, Ko, EY. Role of reactive oxygen species in male infertility: an updated review of literature. Arab J Urol 2018;16:35–43.Google Scholar
De Jonge, CJ. A clinical assay for reactive oxygen species – ready for primetime? Reprod Biomed Online 2018;36:88–9.Google Scholar
Balhorn, R. A model for the structure of chromatin in mammalian sperm. J Cell Biol 1982;93:298–305.Google Scholar
Ward, WS, Coffey, DS. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 1991;44:569–74.Google Scholar
Fuentes-Mascorro, G, Serrano, H, Rosado, A. Sperm chromatin. Arch Androl 2000;45:215–25.Google Scholar
Sakkas, D, Moffatt, O, Manicardi, GC, Mariethoz, E, Tarozzi, N, Bizzaro, D. Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol Reprod 2002;66:1061–7.Google Scholar
Aitken, RJ, De Iuliis, GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod 2010;16:3–13.Google Scholar
Sakkas, D, Alvarez, JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 2010;93:1027–36.Google Scholar
Aitken, RJ, Bronson, R, Smith, TB, De Iuliis, GN. The source and significance of DNA damage in human spermatozoa; a commentary on diagnostic strategies and straw man fallacies. Mol Hum Reprod 2013;19:475–85.Google Scholar
Barratt, CL, Aitken, RJ, Björndahl, L, et al. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications – a position report. Hum Reprod 2010;25:824–38.Google Scholar
Pacey, AA. Environmental and lifestyle factors associated with sperm DNA damage. Hum Fertil 2010;13:189–93.Google Scholar
Evenson, DP, Jost, LK, Marshall, D, et al. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 1999;14:1039–49.Google Scholar
Spanò, M, Bonde, JP, Hjøllund, HI, Kolstad, HA, Cordelli, E, Leter, G. Sperm chromatin damage impairs human fertility. The Danish First Pregnancy Planner Study Team. Fertil Steril 2000;73:43–50.Google Scholar
Evenson, DP, Darzynkiewicz, Z, Melamed, MR. Relation of mammalian sperm chromatin heterogeneity to fertility. Science 1980;210:1131–3.Google Scholar
Evenson, DP, Larson, KL, Jost, LK. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 2002;23:25–43.Google Scholar
Hughes, CM, Lewis, SE, McKelvey-Martin, VJ, Thompson, W. A comparison of baseline and induced DNA damage in human spermatozoa from fertile and infertile men, using a modified comet assay. Mol Hum Reprod 1996;2:613–19.Google Scholar
Hughes, CM, Lewis, SE, McKelvey-Martin, VJ, Thompson, W. Reproducibility of human sperm DNA measurements using the alkaline single cell gel electrophoresis assay. Mutat Res 1997;374:261–8.Google Scholar
Sun, JG, Jurisicova, A, Casper, RF. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997;56:602–7.Google Scholar
Sharma, RK, Sabanegh, E, Mahfouz, R, Gupta, S, Thiyagarajan, A, Agarwal, A. TUNEL as a test for sperm DNA damage in the evaluation of male infertility. Urology 2010;76:1380–6:Google Scholar
Fernández, JL, Muriel, L, Rivero, MT, Goyanes, V, Vazquez, R, Alvarez, JG. The sperm chromatin dispersion test: a simple method for the determination of sperm DNA fragmentation. J Androl 2003;24:59–66.Google Scholar
Fernández, JL, Muriel, L, Goyanes, V, et al. Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion (SCD) test. Fertil Steril 2005;84:833–42.Google Scholar
Fernández, JL, Muriel, L, Goyanes, V, et al. Halosperm® is an easy, available, and cost-effective alternative for determining sperm DNA fragmentation. Fertil Steril 2005;84:860.Google Scholar
Li, Z, Wang, L, Cai, J, Huang, H. Correlation of sperm DNA damage with IVF and ICSI outcomes: a systematic review and meta-analysis. J Assist Reprod Genet 2006;23:367–76.Google Scholar
Evenson, D, Wixon, R. Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod Biomed Online 2006;12:466–72.Google Scholar
Zini, A, Boman, JM, Belzile, E, Ciampi, A. Sperm DNA damage is associate with an increased risk of pregnany after IVF and ICSI: systematic review and meta-analysis. Hum Reprod 2008;23:2663–8.Google Scholar
Shamsi, MB, Imam, SN, Dada, R. Sperm DNA integrity assays: diagnostic and prognostic challenges and implications in management of infertility. J Assist Reprod Genet 2011;28:1073–85.Google Scholar
Robinson, L, Gallos, ID, Conner, SJ, et al. The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum Reprod 2012;27:2908–17.Google Scholar
Zhao, J, Zhang, Q, Wang, Y, Li, Y. Whether sperm deoxyribonucleic acid fragmentation has an effect on pregnancy and miscarriage after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta- analysis. Fertil Steril 2014;102:998–1005Google Scholar
Zhang, Z, Zhu, L, Jiang, H, Chen, H, Chen, Y, Dai, Y. Sperm DNA fragmentation index and pregnancy outcome after IVF or ICSI: a meta-analysis. J Assist Reprod Genet 2015;32:17–26.Google Scholar
Osman, A, Alsomait, H, Seshadri, S, El-Toukhy, T, Khalaf, Y. The effect of sperm DNA fragmentation on live birth rate after IVF or ICSI: a systematic review and meta-analysis. Reprod Biomed Online 2015;30:120–7.Google Scholar
Cissen, M, Wely, MV, Scholten, I, et al. Measuring sperm DNA fragmentation and clinical outcomes of medically assisted reproduction: a systematic review and meta-analysis. PLoS ONE 2016;11:e0165125.Google Scholar
Simon, L, Zini, A, Dyachenko, A, Ciampi, A, Carrell, DT. A systematic review and meta-analysis to determine the effect of sperm DNA damage on in vitro fertilization and intracytoplasmic sperm injection outcome. Asian J Androl 2017;19:80–90.Google Scholar
Pacey, A. Is sperm DNA fragmentation a useful test that identifies a treatable cause of male infertility? Best Pract Res Clin Obstet Gynaecol 2018;53:11–19.Google Scholar
Sugihara, A, Van Avermaete, F, Roelant, E, Punjabi, U, De Neubourg, D. The role of sperm DNA fragmentation testing in predicting intra-uterine insemination outcome: a systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol 2019;244:8–15.Google Scholar
McQueen, DB, Zhang, J, Robins, JC. Sperm DNA fragmentation and recurrent pregnancy loss: a systematic review and meta-analysis. Fertil Steril 2019;112:54–60.Google Scholar
Carrell, DT, De Jonge, CJ. The troubling state of the semen analysis. Andrology 2016;4:761–2.Google Scholar
De Jonge, CJ. Semen analysis: Looking for an upgrade in class. Fertil Steril 2012;97:260–6.Google Scholar
Palermo, G, Joris, H, Devroey, P, Van Steirteghem, AC. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 1992;340:17–18.Google Scholar
Carrell, DT, Nyboe Andersen, A, Lamb, DJ. The need to improve patient care through discriminate use of intracytoplasmic sperm injection (ICSI) and improved understanding of spermatozoa, oocyte and embryo biology. Andrology 2015;3:143–6.Google Scholar
Barratt, CLR, De Jonge, CJ, Sharpe, RM. ‘Man up’: the importance and strategy for placing male reproductive health centre stage in the political and research agenda. Hum Reprod 2018;33:541–45.Google Scholar
Li, Z, Wang, AY, Bowman, M, et al. ICSI does not increase the cumulative live birth rate in non-male factor infertility. Hum Reprod 2018;33:1322–30.Google Scholar
The Practice Committees of the American Society for Reproductive Medicine and Society for Assisted Reproductive Technology. Intracytoplasmic sperm injection (ICSI) for non-male factor infertility: a committee opinion. Fertil Steril 2012;98:1395–9.Google Scholar
De Jonge, C, Barratt, CLR. The present crisis in male reproductive health: an urgent need for a political, social, and research roadmap. Andrology 2019;7:762–8.Google Scholar
Barratt, CLR, Björndahl, L, De Jonge, CJ, et al. The diagnosis of male infertility: an analysis of the evidence to support the development of global WHO guidance – challenges and future research opportunities. Hum Reprod Update 2017;23:660–80.Google Scholar
Esteves, SC, Roque, M, Bedoschi, G, Haahr, T, Humaidan, P. Intracytoplasmic sperm injection for male infertility and consequences for offspring. Nat Rev Urol 2018;15:535–62.Google Scholar
Barratt, CL, Anderson, RA, De Jonge, C. Male fertility: a window on the health of this generation and the next. Reprod Biomed Online 2019;39:721–3.Google Scholar