Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T22:12:31.008Z Has data issue: false hasContentIssue false

Section 4 - Laboratory Evaluation and Treatment of Male Infertility

Published online by Cambridge University Press:  06 December 2023

Edited by
Douglas T. Carrell ,
Alexander W. Pastuszak  and
James M. Hotaling
Douglas T. Carrell
Affiliation:
Utah Center for Reproductive Medicine
Alexander W. Pastuszak
Affiliation:
University of Utah
James M. Hotaling
Affiliation:
Utah Center for Reproductive Medicine
Get access
Type
Chapter
Information
Men's Reproductive and Sexual Health Throughout the Lifespan
An Integrated Approach to Fertility, Sexual Function, and Vitality
 , pp. 159 - 250
Publisher: Cambridge University Press
Print publication year: 2023

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

References

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;23:660–680.CrossRefGoogle ScholarPubMed
Keel, BA. How reliable are results from the semen analysis? Fertil Steril. 2004;82:41–44.CrossRefGoogle ScholarPubMed
Björndahl, L, Barratt, CL, Mortimer, D, Jouannet, P. ‘How to count sperm properly’: checklist for acceptability of studies based on human semen analysis. Hum Reprod (Oxford). 2016;31:227–232.Google ScholarPubMed
van Leeuwenhoek, A. Observationes D. Anthonii Lewenhoeck, de natis’e semine genitali animalculis. Philos Trans R Soc Lond B Biol Sci. 1677;12:1040–1046.Google Scholar
Harvey, C, Jackson, MH. Assessment of male fertility by semen analysis – an attempt to standardise methods. Lancet. 1945:99–104.CrossRefGoogle Scholar
MacLeod, J, Hotchkiss, RS. The distribution of spermatozoa and of certain chemical constituents in the human ejaculate. J Urology. 1942;48:225–229.Google Scholar
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;1:347–361.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.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 Urology. 1951;66:436–449.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. The biochemistry of the human male genital tract. Int Rec Med Gen Pract Clin. 1951;164:671–673.Google Scholar
MacLeod, J. Effect of chickenpox and of pneumonia on semen quality. Fertil Steril. 1951;2:523–533.CrossRefGoogle ScholarPubMed
MacLeod, J. Semen quality in 1000 men of known fertility and in 800 cases of infertile marriage. Fertil Steril. 1951;2:115–139.Google Scholar
MacLeod, J. Sulfhydryl groups in relation to the metabolism and motility of human spermatozoa. J Gen Physiol. 1951;34:705–714.Google Scholar
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. V. Effect of continence on semen quality. Fertil Steril. 1952;3:297–315.Google Scholar
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. VI. Semen quality and certain other factors in relation to ease of conception. Fertil Steril. 1953;4:10–33.CrossRefGoogle ScholarPubMed
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. VII. Semen quality in relation to age and sexual activity. Fertil Steril. 1953;4:194–209.Google Scholar
Gold, RZ, Macleod, J. The male factor in fertility and infertility. VIII. A study of variation in semen quality. Fertil Steril. 1956;7:387–410.Google ScholarPubMed
MacLeod, J, Gold, RZ. The male factor in fertility and infertility. IX. Semen quality in relation to accidents of pregnancy. Fertil Steril. 1957;8:36–49.Google Scholar
Eliasson, R. Analysis of semen. In: Behrman, SJ, Kistner, RW, eds. Progress in Infertility. Little, Brown and Co; 1975:691–713.Google Scholar
Eliasson, R. Semen analysis and laboratory workup. In: Cockett, ATK, Urry, RL, eds. Male Infertility Workup, Treatment and Research. Grune & Stratton; 1977:169–188.Google Scholar
Eliasson, R. Analysis of semen. In: Burger, HG, De Kretser, DM, eds. The Testis. Raven Press; 1981:381–399.Google Scholar
Arver, S, Kvist, U, Bjorndahl, L. In memoriam: Rune Eliasson MD, PhD. Andrology. 2020;8:530–531.CrossRefGoogle Scholar
Mortimer, D. Laboratory standards in routine clinical andrology. Reprod Med Rev. 1994;3:97–111.Google Scholar
Mortimer, D. Practical Laboratory Andrology. Oxford University Press; 1994.Google Scholar
Björndahl, L, Barratt, CL, Fraser, LR, Kvist, U, Mortimer, D. ESHRE Basic Semen Analysis Courses 1995–1999: immediate beneficial effects of standardized training. Hum Reprod (Oxford). 2002;17:1299–1305.Google Scholar
Barratt, CL, Björndahl, L, Menkveld, R, Mortimer, D. ESHRE Special Interest Group For Andrology Basic Semen Analysis Course: a continued focus on accuracy, quality, efficiency and clinical relevance. Hum Reprod (Oxford). 2011;26:3207–3212.CrossRefGoogle ScholarPubMed
Mortimer, D, Björndahl, L, Barratt, CLR, et al. A Practical Guide to Basic Laboratory Andrology. 2nd ed. Cambridge University Press; 2022.Google Scholar
Belsey, M, Eliasson, R, Gallegos, AJ, Moghissi, KS, Paulsen, CA, Prassad, AMN. Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction. Press Concern; 1980.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interactions. 2nd ed. Cambridge University Press; 1987.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interactions. 3rd ed. Cambridge University Press; 1992.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interactions. 4th ed. Cambridge University Press; 1999.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th ed. World Health Organization; 2010.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen. 6th ed. World Health Organization; 2021.Google Scholar
Eisenberg, ML, Li, S, Behr, B, et al. Semen quality, infertility and mortality in the USA. Hum Reprod (Oxford). 2014;29:1567–1574.Google Scholar
Punjabi, U, Spiessens, C. Basic Semen Analysis Courses: experience in Belgium. In: Ombelet, W, Bosmans, E, Vandeput, H, Vereecken, A, Renier, M, Hoomans, E, eds. Modern ART in the 2000s: Andrology in the Nineties. The Parthenon Publishing Group; 1998:107–113.Google Scholar
Vreeburg, JTM, Weber, RFA. Basic Semen Analysis Courses: experience in the Netherlands. In: Ombelet, W, Bosmans, E, Vandeput, H, Vereecken, A, Renier, M, Hoomans, E, eds. Modern ART in the 2000s: Andrology in the Nineties. The Parthenon Publishing Group; 1998:103–106.Google Scholar
Mortimer, D, Shu, MA, Tan, R. Standardization and quality control of sperm concentration and sperm motility counts in semen analysis. Hum Reprod (Oxford). 1986;1:299–303.Google Scholar
Cooper, TG, Neuwinger, J, Bahrs, S, Nieschlag, E. Internal quality control of semen analysis. Fertil Steril. 1992;58:172–178.Google Scholar
Cooper, TG, Björndahl, L, Vreeburg, J, Nieschlag, E. Semen analysis and external quality control schemes for semen analysis need global standardization. Int J Androl. 2002;25:306–311.Google Scholar
Björndahl, L. What is normal semen quality? On the use and abuse of reference limits for the interpretation of semen analysis results. Hum Fertil (Camb). 2011;14:179–186.Google Scholar
Pound, N, Javed, MH, Ruberto, C, Shaikh, MA, Del Valle, AP. Duration of sexual arousal predicts semen parameters for masturbatory ejaculates. Physiol Behav. 2002;76:685–689.CrossRefGoogle ScholarPubMed
Amann, RP. Considerations in evaluating human spermatogenesis on the basis of total sperm per ejaculate. J Androl. 2009;30:626–641.Google Scholar
Björndahl, L, Kvist, U. Sequence of ejaculation affects the spermatozoon as a carrier and its message. Reprod Biomed Online. 2003;7:440–448.CrossRefGoogle ScholarPubMed
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. Syst Biol Reprod Med. 2011;57:86–92.Google Scholar
Eisenberg, ML, Walsh, TJ, Garcia, MM, Shinohara, K, Turek, PJ. Ejaculatory duct manometry in normal men and in patients with ejaculatory duct obstruction. J Urology. 2008;180:255–260; discussion 60.CrossRefGoogle ScholarPubMed
Björndahl, L. Semen characteristics and aging: technical considerations regarding variability. In: Carrell, D, ed. Paternal Influences on Human Reproductive Success. Cambridge University Press; 2013:183–190.Google Scholar
Cooper, TG, Brazil, C, Swan, SH, Overstreet, JW. Ejaculate volume is seriously underestimated when semen is pipetted or decanted into cylinders from the collection vessel. J Androl. 2007;28:1–4.Google Scholar
Björndahl, L, Mortimer, D, Barratt, CLR, et al. A Practical Guide to Basic Laboratory Andrology. Cambridge University Press; 2010.CrossRefGoogle Scholar
Mortimer, D. A technical note on the assessment of human sperm vitality using eosin-nigrosin staining. Reprod Biomed Online. 2020;40:851–855.CrossRefGoogle ScholarPubMed

References

Mortimer, ST. A critical review of the physiological importance and analysis of sperm movement in mammals. Hum Reprod Update. 1997;3:403–439.Google Scholar
Björndahl, L, Mortimer, D, Barratt, CLR, et al. A Practical Guide to Basic Laboratory Andrology. Cambridge University Press; 2010.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
Mortimer, D. Objective analysis of sperm motility and kinematics. In: Keel, BA, Webster, BW, eds. Handbook of the Laboratory Diagnosis and Treatment of Infertility. CRC Press; 1990:97–133.Google Scholar
Mortimer, D. Practical Laboratory Andrology. Oxford University Press; 1994.CrossRefGoogle Scholar
David, G, Serres, C, Jouannet, P. Kinematics of human spermatozoa. Gamete Res. 1981;4:83–95.Google Scholar
Mortimer, D, Mortimer, ST. Value and reliability of CASA systems. In: Ombelet, W, Bosmans, E, Vandeput, H, Vereecken, A, Renier, M, Hoomans, EH, eds. Modern ART in the 2000’s: Andrology in the Nineties. Parthenon Publishing, 1998:73–89.Google Scholar
Mortimer, D, Aitken, RJ, Mortimer, ST, Pacey, AA. Clinical CASA: the quest for consensus. Reprod Fertil Dev. 1995;7:951–959.CrossRefGoogle ScholarPubMed
Mortimer, D, Mortimer, ST. Routine application of CASA in human clinical andrology and ART laboratories. In: Flanagan, J, Björndahl, L, Kvist, U, eds. Proceedings of the 13th International Symposium on Spermatology. Springer Nature Switzerland AG, 2018:183–197.Google Scholar
ESHRE Andrology Special Interest Group. Guidelines on the application of CASA technology in the analysis of spermatozoa. Hum Reprod. 1998;13:142–145.Google Scholar
Mortimer, ST van der Horst, G, Mortimer, D. The future of computer‐aided sperm analysis. Asian J Androl. 2015;17:545–553.Google Scholar
Sanders, D, Fensome-Rimmer, S, Woodward, B. Uncertainty of measurement in andrology: UK best practice guideline from the Association of Biomedical Andrologists. Br J Biomed Sci. 2017;74:157–162.Google Scholar
Yeste, M, Bonet, S, Rodríguez-Gil, JE, Rivera Del Álamo, MM. Evaluation of sperm motility with CASA-Mot: which factors may influence our measurements? Reprod Fertil Dev. 2018;30:789–798.Google Scholar
Schubert, B, Badiou, M, Force, A. Computer-aided sperm analysis, the new key player in routine sperm assessment. Andrologia. 2019;51:e13417.Google Scholar
Douglas-Hamilton, DH, Smith, NG, Kuster, CE, Vermeiden, JP, Althouse, GC. Particle distribution in low-volume capillary-loaded chambers. J Androl. 2005;26:107–114.Google Scholar
Douglas-Hamilton, DH, Smith, NG, Kuster, CE, Vermeiden, JP, Althouse, GC. Capillary-loaded particle fluid dynamics: effect on estimation of sperm concentration. J Androl. 2005;26:115–122.Google Scholar
Mortimer, D. Sperm transport in the female genital tract. In: Grudzinskas, JG, Yovich, JL, eds. Cambridge Reviews in Human Reproduction, Volume 2: Gametes – The Spermatozoon. Cambridge University Press; 1995:157–174.Google Scholar
Björndahl, L, Barratt, CLR, Mortimer, D, Jouannet, P. How to count sperm properly: checklist for acceptability of studies based on human semen analysis. Hum Reprod. 2016;31:227–232.Google ScholarPubMed
Dearing, C, Jayasena, C, Lindsay, K. Can the Sperm Class Analyser (SCA) CASA-Mot system for human sperm motility analysis reduce imprecision and operator subjectivity and improve semen analysis? Hum Fertil (Camb). 2021;24(3):208–218.Google Scholar
Tomlinson, MJ, Naeem, A. CASA in the medical laboratory: CASA in diagnostic andrology and assisted conception. Reprod Fertil Dev. 2018;30:850–859.Google Scholar
Lammers, J, Splingart, C, Barrière, P, Jean, M, Fréour, T. Double-blind prospective study comparing two automated sperm analyzers versus manual semen assessment. J Assist Reprod Genet. 2014;31:35–43.Google Scholar
Dearing, CG, Kilburn, S, Lindsay, KS. Validation of the sperm class analyser CASA system for sperm counting in a busy diagnostic semen analysis laboratory. Hum Fertil. 2014;17:37–44.Google Scholar
Agarwal, A, Henkel, R, Huang, C-C, Lee, M-S. Automation of human semen analysis using a novel artificial intelligence optical microscopic technology. Andrologia. 2019;51:e13440.Google Scholar
Cooper, TG, Noonan, E, von Eckardstein, S, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update. 2010;16:231–245.Google Scholar
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th ed. World Health Organization; 2010.Google Scholar
Björndahl, L. What is normal semen quality? On the use and abuse of reference limits for the interpretation of semen analysis results. Hum Fertil. 2011;14:179–186.CrossRefGoogle ScholarPubMed
Mortimer, ST. CASA – practical aspects. J Androl. 2000;21:515–524.CrossRefGoogle ScholarPubMed
Barratt, CLR, Björndahl, L, Menkveld, R, Mortimer, D. The ESHRE Special Interest Group for Andrology Basic Semen Analysis Course: a continued focus on accuracy, quality, efficiency and clinical relevance. Hum Reprod. 2011;26:3207–3212.CrossRefGoogle ScholarPubMed
Mortimer, D, Mortimer, ST. Laboratory investigation of the infertile male. In: Brinsden, PR, ed. A Textbook of In-Vitro Fertilization and Assisted Reproduction. 3rd ed. Taylor & Francis Medical Books; 2005:61–91.Google Scholar
Mortimer, D, Mortimer, ST. Computer-aided sperm analysis (CASA) of sperm motility and hyperactivation. In: Carrell, DT, Aston, KI, eds. Spermatogenesis and Spermiogenesis: Methods and Protocols. Methods in Molecular Biology 927. Springer (Humana Press); 2013:77–87.Google Scholar
ESHRE Special Interest Group of Embryology and Alpha Scientists in Reproductive Medicine. The Vienna Consensus: report of an expert meeting on the development of ART laboratory performance indicators. Reprod Biomed Online. 2017;35:494–510.Google Scholar
Mortimer, ST, Schoëvaërt, D, Swan, MA, Mortimer, D. Quantitative observations of flagellar motility of capacitating human spermatozoa. Hum Reprod. 1997;12:1006–1012.Google Scholar
Alasmari, W, Barratt, CLR, Publicover, SJ, et al. The clinical significance of calcium signaling pathways mediating human sperm hyperactivation. Hum Reprod. 2013;28:866–876.CrossRefGoogle ScholarPubMed
Mortimer, D, Serres, C, Mortimer, ST, Jouannet, P. Influence of image sampling frequency on the perceived movement characteristics of progressively motile human spermatozoa. Gamete Res. 1988;20:313–327.Google Scholar
Mortimer, D. Structured management as a basis for cost-effective infertility care. In: Gagnon, C, ed. The Male Gamete: From Basic Knowledge to Clinical Applications. Cache River Press; 1999:363–370.Google Scholar
Rowe, PJ, Comhaire, FH, Hargreave, TB, Mahmoud, AMA. WHO Clinical Manual for the Standardized Investigation, Diagnosis and Management of the Infertile Male. Cambridge University Press; 2000.Google Scholar
Mortimer, D, Mortimer, ST. The case against intracytoplasmic sperm injection for all. In: Aitken, J, Mortimer, D, Kovacs, G, eds. Male and Sperm Factors That Maximize IVF Success. Cambridge University Press; 2020:130–140.Google Scholar
Mortimer, D, Menkveld, R. Sperm morphology assessment: historical perspectives and current opinions. J Androl. 2001;22:192–205.Google Scholar
Mortimer, D. Sperm form and function: beauty is in the eye of the beholder. In: van der Horst, G, Franken, D, Bornman, R, de Jager, T, Dyer, S, eds. Proceedings of 9th International Symposium on Spermatology. Monduzzi Editore; 2002:257–262.Google Scholar
Auger, J, Jouannet, P, Eustache, F. Another look at human sperm morphology. Hum Reprod. 2016;31:10–23.Google Scholar
Gatimel, N, Moreau, J, Parinaud, J, Léandri, RD. Sperm morphology: assessment, pathophysiology, clinical relevance, and state of the art in 2017. Andrology. 2017;5:845–862.Google Scholar
Mortimer, D. The functional anatomy of the human spermatozoon: relating ultrastructure and function. Mol Hum Reprod. 2018;24:567–592.Google Scholar
Coetzee, K, Kruger, TF, Lombard, CJ. Repeatability and variance analysis on multiple computer-assisted (IVOS) sperm morphology readings. Andrologia. 1999;31:163–168.Google Scholar
Mortimer, D. A technical note on the assessment of human sperm vitality using eosin-nigrosin staining. Reprod Biomed Online. 2020;40:851–855.Google Scholar
Mortimer, D, Curtis, EF, Camenzind, AR, Tanaka, S. The spontaneous acrosome reaction of human spermatozoa incubated in vitro. Hum Reprod. 1989;4:57–62.Google Scholar
Sadeghi, S, García-Molina, A, Celma, F, Valverde, A, Fereidounfar, S, Soler, C. Morphometric comparison by the ISAS® CASA-DNAf system of two techniques for the evaluation of DNA fragmentation in human spermatozoa. Asian J Androl. 2016;18:835–839.Google Scholar
ESHRE Andrology Special Interest Group. Consensus workshop on advanced diagnostic andrology techniques. Hum Reprod. 1996;11:1463–1479.Google Scholar
Mortimer, D, Curtis, EF, Miller, RG. Specific labelling by peanut agglutinin of the outer acrosomal membrane of the human spermatozoon. J Reprod Fertil. 1987;81:127–135.Google Scholar
Mortimer, D, Goel, N, Shu, MA. Evaluation of the CellSoft automated semen analysis system in a routine laboratory setting. Fertil Steril. 1988;50:960–968.Google Scholar
Bland, JM, Altman, DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986;1:307–310.Google Scholar
International Standards Organization. ISO 15189:2012 Medical laboratories – Requirements for quality and competence. International Standards Organization; 2012.Google Scholar
International Standards Organization. ISO/TS 20914:2019 Medical laboratories – Practical guidance for the estimation of measurement uncertainty. International Standards Organization; 2019.Google Scholar
International Standards Organization. ISO 23162:2021 Basic semen examination – Specification and test methods. International Standards Organization; 2021.Google Scholar

References

Duca, Y, Calogero, AE, Cannarella, R, Condorelli, RA, La Vignera, S. Current and emerging medical therapeutic agents for idiopathic male infertility. Expert Opin Pharmacother. 2019;20(1):55–67.CrossRefGoogle ScholarPubMed
Nicopoullos, J, Vicens-Morton, A, Lewis, S, et al. Novel use of COMET parameters of sperm DNA damage may increase its utility to diagnose male infertility and predict live births following both IVF and ICSI. Hum Reprod. 2019;151:1–9.Google Scholar
Dada, R. Sperm DNA damage diagnostics: when and why. Transl Androl Urol. 2017;6(4):S691–S694.Google Scholar
Bui, AD, Sharma, R, Henkel, R, Agarwal, A. Reactive oxygen species impact on sperm DNA and its role in male infertility. Andrologia. 2018;50(8): e13012.Google Scholar
Sakkas, D, Seli, E, Bizzaro, D, Tarozzi, N, Manicardi, GC. Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. Reprod Biomed Online. 2003;7(4):428–432.Google Scholar
Esteves, SC, Santi, D, Simoni, M. An update on clinical and surgical interventions to reduce sperm DNA fragmentation in infertile men. Andrology. 2020;8(1):53–81.Google Scholar
Panner Selvam, MK, Ambar, RF, Agarwal, A, Henkel, R. Etiologies of sperm DNA damage and its impact on male infertility. Andrologia. 2021;53(1): e13706.Google Scholar
Cissen, M, Van Wely, M, 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(11):e0165125.Google Scholar
Brandt, JS, Cruz Ithier, MA, Rosen, T, Ashkinadze, E. Advanced paternal age, infertility, and reproductive risks: a review of the literature. Prenat Diagn. 2019;39(2):81–87.Google Scholar
Horta, F, Vollenhoven, B, Healey, M, Busija, L, Catt, S, Temple-Smith, P. Male ageing is negatively associated with the chance of live birth in IVF/ICSI cycles for idiopathic infertility. Hum Reprod. 2019;34(12):2523–2532.Google Scholar
Ramasamy, R, Chiba, K, Butler, P, Lamb, DJ. Male biological clock: a critical analysis of advanced paternal age. Fertil Steril. 2015;103(6):1402–1406.Google Scholar
van Kooij, RJ, de Boer, P, de Vreeden-Elbertse, JMT, Ganga, NA, Singh, N, te Velde, ER. The neutral comet assay detects double strand DNA damage in selected and unselected human spermatozoa of normospermic donors. Int J Androl. 2004;27(3):140–146.Google Scholar
Hoeijmakers, JHJ. Genome maintenance mechanisms for preventing cancer. Nature. 2001;411(6835):366–374.CrossRefGoogle ScholarPubMed
Agarwal, A, Saleh, RA, Bedaiwy, MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003;79(4):829–843.Google Scholar
Shamsi, MB, Kumar, R, Dada, R. Evaluation of nuclear DNA damage in human spermatozoa in men opting for assisted reproduction. Indian J Med Res. 2008;127(2):115–123.Google Scholar
Horta, F, Catt, S, Vollenhoven, B, Temple-Smith, P. Oocyte DNA repair capacity of controlled sperm DNA damage is affected by female age. Hum Reprod. 2018;33(2):529–544.Google Scholar
Vyas, L, Lewis, S, Tharakan, T, Jayasena, C, Minhas, S, Ramsay, J. MP75–01 evidence that testicular sperm has improved DNA integrity compared to ejaculated sperm in infertile men. J Urol. 2019;201(4).Google Scholar
Lopes, LS, Esteves, SC. Testicular sperm in non-azoospermic infertile men with oxidatively induced high sperm DNA damage. In: Parekattil, S, Esteves, S, Agarwal, A, eds. Male Infertility. Springer International Publishing; 2020:735–745.Google Scholar
Lewis, SEM, Kumar, K. The paternal genome and the health of the assisted reproductive technology child. Asian J Androl. 2015;17(4):616–622.Google Scholar
Simon, L, Emery, BR, Carrell, DT. Review: diagnosis and impact of sperm DNA alterations in assisted reproduction. Best Pract Res Clin Obstet Gynaecol. 2017;44:38–56.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(1):54–60.e3.Google Scholar
Borges, E, Zanetti, BF, Setti, AS, Braga, DP de AF, Provenza, RR, Iaconelli, A. Sperm DNA fragmentation is correlated with poor embryo development, lower implantation rate, and higher miscarriage rate in reproductive cycles of non-male factor infertility. Fertil Steril. 2019;112(3):483–490.Google Scholar
Wdowiak, A, Bakalczuk, S, Bakalczuk, G. The effect of sperm DNA fragmentation on the dynamics of the embryonic development in intracytoplasmatic sperm injection. Reprod Biol. 2015;15(2):94–100.Google Scholar
Wright, C, Milne, S, Leeson, H. Sperm DNA damage caused by oxidative stress: modifiable clinical, lifestyle and nutritional factors in male infertility. Reprod Biomed Online. 2014;28(6):684-703.Google Scholar
Samuel, R, Feng, H, Jafek, A, Despain, D, Jenkins, T, Gale, B. Microfluidic-based sperm sorting & analysis for treatment of male infertility. Transl Androl Urol. 2018;7(3):S336–S347.CrossRefGoogle ScholarPubMed
Kishi, K, Ogata, H, Ogata, S, et al. Frequency of sperm DNA fragmentation according to selection method: comparison and relevance of a microfluidic device and a swim-up procedure. J Clin Diagn Res. 2015;9(11):QC14–QC16.Google Scholar
Yildiz, K, Yuksel, S. Use of microfluidic sperm extraction chips as an alternative method in patients with recurrent in vitro fertilisation failure. J Assist Reprod Genet. 2019;36(7):1423–1429.Google Scholar
Esteves, SC, Roque, M. Extended indications for sperm retrieval: summary of current literature. F1000Research. 2019;8.Google Scholar
Zhang, J, Xue, H, Qiu, F, Zhong, J, Su, J. Testicular spermatozoon is superior to ejaculated spermatozoon for intracytoplasmic sperm injection to achieve pregnancy in infertile males with high sperm DNA damage. Andrologia. 2019;51(2):e13175.Google Scholar
Drevet, JR, Aitken, RJ. Oxidation of sperm nucleus in mammals: a physiological necessity to some extent with adverse impacts on oocyte and offspring. Antioxidants. 2020;9(2):95.Google Scholar
Martin-Hidalgo, D, Bragado, MJ, Batista, AR, Oliveira, PF, Alves, MG. Antioxidants and male fertility: from molecular studies to clinical evidence. Antioxidants. 2019;8(4):89.Google Scholar
Sanocka, D, Kurpisz, M. Reactive oxygen species and sperm cells. Reprod Biol Endocrinol. 2004;2(1):1–7.CrossRefGoogle ScholarPubMed
Aktan, G, Doǧru-Abbasoǧlu, S, Küçükgergin, C, Kadioǧlu, A, Özdemirler-Erata, G, Koçak-Toker, N. Mystery of idiopathic male infertility: is oxidative stress an actual risk? Fertil Steril. 2013;99(5):1211–1215.Google Scholar
Khosravi, F, Valojerdi, MR, Amanlou, M, Karimian, L, Abolhassani, F. Relationship of seminal reactive nitrogen and oxygen species and total antioxidant capacity with sperm DNA fragmentation in infertile couples with normal and abnormal sperm parameters. Andrologia. 2014;46(1):17–23.Google Scholar
Shamsi, MB, Kumar, R, Malhotra, N, et al. Chromosomal aberrations, Yq microdeletion, and sperm DNA fragmentation in infertile men opting for assisted reproduction. Mol Reprod Dev. 2012;79(9):637–650.Google Scholar
Aitken, RJ, Jones, KT, Robertson, SA. Reactive oxygen species and sperm function-in sickness and in health. J Androl. 2012;33(6):1096–1106.Google Scholar
O’Flaherty, C. Reactive oxygen species and male fertility. Antioxidants. 2020;9(4):287.Google Scholar
Wright, C, Milne, S, Leeson, H. Sperm DNA damage caused by oxidative stress: modifiable clinical, lifestyle and nutritional factors in male infertility. Reprod Biomed Online. 2014;28(6):684–703.Google Scholar
Lewis, SEM, Boyle, PM, McKinney, KA, Young, IS, Thompson, W. Total antioxidant capacity of seminal plasma is different in fertile and infertile men. Fertil Steril. 1995;64(4):868–870.Google Scholar
Lewis, SEM, Samantha Sterling, EL, Young, IS, Thompson, W. Comparison of individual antioxidants of sperm and seminal plasma in fertile and infertile men. Fertil Steril. 1997;67(1):142–147.Google Scholar
Mylonas, C, Kouretas, D. Lipid peroxidation and tissue damage. In Vivo (Brooklyn). 1999;13(3):295–309.Google ScholarPubMed
Atig, F, Raffa, M, Ben Ali, H, Abdelhamid, K, Saad, A, Ajina, M. Altered antioxidant status and increased lipid per-oxidation in seminal plasma of Tunisian infertile men. Int J Biol Sci. 2011;8(1):139–149.Google Scholar
Sanocka, D, Kurpisz, M. Reactive oxygen species and sperm cells. Reprod Biol Endocrinol. 2004;2:12.Google Scholar
Badouard, C, Ménézo, Y, Panteix, G, et al. Determination of new types of DNA lesions in human sperm. Zygote. 2008;16(1):9–13.Google Scholar
Lamirande, E De, Jiang, H, Zini, A, Kodama, H, Gagnon, C. Reactive oxygen species and sperm physiology. Rev Reprod. 1997;2(1):48–54.Google Scholar
Oehninger, S, Blackmore, P, Mahony, M, Hodgen, G. Effects of hydrogen peroxide on human spermatozoa. J Assist Reprod Genet. 1995;12(1):41–47.Google Scholar
Martins da Silva, SJ. Male infertility and antioxidants: one small step for man, no giant leap for andrology? Reprod Biomed Online. 2019;39(6):879–883.Google Scholar
Smits, RM, Mackenzie-Proctor, R, Yazdani, A, Stankiewicz, MT, Jordan, V, Showell, MG. Antioxidants for male subfertility. Cochrane Database Syst Rev. 2019;3(3):CD007411.Google Scholar
Agarwal, A, Parekh, N, Selvam, MKP, et al. Male oxidative stress infertility (MOSI): proposed terminology and clinical practice guidelines for management of idiopathic male infertility. World J Mens Health. 2019;37(3):296–312.Google Scholar
Ritchie, C, Ko, EY. Oxidative stress in the pathophysiology of male infertility. Andrologia. 2020;53(1):e13581.Google Scholar

References

Cooper, TG, Noonan, E, von Eckardstein, S, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update. 2010;16(3):231–245.Google Scholar
Vinnakota, C, Cree, L, Peek, J, Morbeck, DE. Incidence of high sperm DNA fragmentation in a targeted population of subfertile men. Syst Biol Reprod Med. 2019;65(6):451–457.Google Scholar
Fernández-Gonzalez, R, Moreira, PN, Pérez-Crespo, M, et al. Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol Reprod. 2008;78(4):761–772.Google Scholar
Bungum, M, Bungum, L, Lynch, KF, Wedlund, L, Humaidan, P, Giwercman, A. Spermatozoa DNA damage measured by sperm chromatin structure assay (SCSA) and birth characteristics in children conceived by IVF and ICSI. Int J Androl. 2012;35(4):485–490.Google Scholar
Ji, BT, Shu, XO, Linet, MS, et al. Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst. 1997;89(3):238–244.Google Scholar
Al-Jebari, Y, Glimelius, I, Berglund Nord, C, et al. Cancer therapy and risk of congenital malformations in children fathered by men treated for testicular germ-cell cancer: a nationwide register study. PLoS Med. 2019;16(6):e1002816.Google Scholar
Zini, A, Sigman, M. Are tests of sperm DNA damage clinically useful? Pros and cons. J Androl. 2009;30(3):219–229.Google Scholar
De Iuliis, GN, Thomson, LK, Mitchell, LA, et al. DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2’-deoxyguanosine, a marker of oxidative stress. Biol Reprod. 2009;81(3):517–524.Google Scholar
Suganuma, R, Yanagimachi, R, Meistrich, ML. Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Hum Reprod. 2005;20(11):3101–3108.Google Scholar
Muratori, M, Marchiani, S, Tamburrino, L, Baldi, E. Sperm DNA fragmentation: mechanisms of origin. Adv Exp Med Biol. 2019;1166:75–85.Google Scholar
Moskovtsev, SI, Willis, J, White, J, Mullen, JB. Sperm DNA damage: correlation to severity of semen abnormalities. Urology. 2009;74(4):789–793.CrossRefGoogle ScholarPubMed
Johnson, L. Spermatogenesis and aging in the human. J Androl. 1986;7(6):331–354.Google Scholar
Sartorius, GA, Nieschlag, E. Paternal age and reproduction. Hum Reprod Update. 2010;16(1):65–79.Google Scholar
Belloc, S, Benkhalifa, M, Cohen-Bacrie, M, Dalleac, A, Amar, E, Zini, A. Sperm DNA damage in normozoospermic men is related to age and sperm progressive motility. Fertil Steril. 2014;101(6):1588–1593.Google Scholar
Wyrobek, AJ, Eskenazi, B, Young, S, et al. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci U S A. 2006;103(25):9601–9606.Google Scholar
Yatsenko, AN, Turek, PJ. Reproductive genetics and the aging male. J Assist Reprod Genet. 2018;35(6):933–941.Google Scholar
Smit, M, van Casteren, NJ, Wildhagen, MF, Romijn, JC, Dohle, GR. Sperm DNA integrity in cancer patients before and after cytotoxic treatment. Hum Reprod. 2010;25(8):1877–1883.Google Scholar
Ståhl, O, Eberhard, J, Cavallin-Ståhl, E, et al. Sperm DNA integrity in cancer patients: the effect of disease and treatment. Int J Androl. 2009;32(6):695–703.Google Scholar
Bujan, L, Walschaerts, M, Moinard, N, et al. Impact of chemotherapy and radiotherapy for testicular germ cell tumors on spermatogenesis and sperm DNA: a multicenter prospective study from the CECOS network. Fertil Steril. 2013;100(3):673–680.Google Scholar
Brydøy, M, Fosså, SD, Klepp, O, et al. Norwegian Urology Cancer Group (NUCG) III study group. Sperm counts and endocrinological markers of spermatogenesis in long-term survivors of testicular cancer. Br J Cancer. 2012;107(11):1833–1839.Google Scholar
Paoli, D, Gallo, M, Rizzo, F, et al. Testicular cancer and sperm DNA damage: short- and long-term effects of antineoplastic treatment. Andrology. 2015;3(1):122–128.Google Scholar
Robbins, WA, Meistrich, ML, Moore, D, et al. Chemotherapy induces transient sex chromosomal and autosomal aneuploidy in human sperm. Nat Genet. 1997;16(1):74–78.Google Scholar
Martin, RH, Ernst, S, Rademaker, A, et al. Chromosomal abnormalities in sperm from testicular cancer patients before and after chemotherapy. Hum Genet. 1997;99(2):214–218.Google Scholar
Lee, SJ, Schover, LR, Partridge, AH, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24(18):2917–2931.Google Scholar
Krishnamurthy, H, Kumar, KM, Joshi, CV, Krishnamurthy, HN, Moudgal, RN, Sairam, MR. Alterations in sperm characteristics of follicle-stimulating hormone (FSH)-immunized men are similar to those of FSH-deprived infertile male bonnet monkeys. J Androl. 2000;21(2):316–327.Google Scholar
Xing, W, Krishnamurthy, H, Sairam, MR. Role of follitropin receptor signaling in nuclear protein transitions and chromatin condensation during spermatogenesis. Biochem Biophys Res Commun. 2003;312(3):697–701.Google Scholar
Meeker, JD, Singh, NP, Hauser, R. Serum concentrations of estradiol and free T4 are inversely correlated with sperm DNA damage in men from an infertility clinic. J Androl. 2008;29(4):379–388.Google Scholar
Erenpreiss, J, Hlevicka, S, Zalkalns, J, Erenpreisa, J. Effect of leukocytospermia on sperm DNA integrity: a negative effect in abnormal semen samples. J Androl. 2002;23(5):717–723.CrossRefGoogle ScholarPubMed
La Vignera, S, Condorelli, R, D’Agata, R, Vicari, E, Calogero, AE. Semen alterations and flow-citometry evaluation in patients with male accessory gland infections. J Endocrinol Invest. 2012;35(2):219–223.Google Scholar
Gallegos, G, Ramos, B, Santiso, R, Goyanes, V, Gosálvez, J, Fernández, JL. Sperm DNA fragmentation in infertile men with genitourinary infection by chlamydia trachomatis and mycoplasma. Fertil Steril. 2008;90(2):328–334.Google Scholar
Cortés‐Gutiérrez, EI, Dávila‐Rodríguez, MI, Fernández, JL, de la O‐Pérez, LO,Garza‐Flores, ME, Eguren-Garza, R,Gosálvez, J. The presence of human papillomavirus in semen does not affect the integrity of sperm DNA. Andrologia. 2017;49(10):e12774.Google Scholar
Damsgaard, J, Joensen, UN, Carlsen, E, et al. Varicocele is associated with impaired semen quality and reproductive hormone levels: a study of 7035 healthy young men from six European countries. Eur Urol. 2016;70(6):1019–1029.Google Scholar
Zini, A, Dohle, G. Are varicoceles associated with increased deoxyribonucleic acid fragmentation? Fertil Steril. 2011;96(6):1283–1287.Google Scholar
Roque, M, Esteves, SC. Effect of varicocele repair on sperm DNA fragmentation: a review. Int Urol Nephrol. 2018;50(4):583–603.Google Scholar
Smith, R, Kaune, H, Parodi, D, et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod. 2006;21(4):986–993.Google Scholar
Kaufman, DW, Kelly, JP, Rosenberg, L, Anderson, TE, Mitchell, AA. Effect of prescriber education on the use of medications contraindicated in older adults in a managed Medicare population. JAMA. 2002;287(3):337–344.Google Scholar
Kantor, ED, Rehm, CD, Haas, JS, Chan, AT, Giovannucci, EL. Trends in prescription drug use among adults in the United States from 1999–2012. JAMA. 2015;314(17):1818–1831.Google Scholar
Safarinejad, MR. Sperm DNA damage and semen quality impairment after treatment with selective serotonin reuptake inhibitors detected using semen analysis and sperm chromatin structure assay. J Urol. 2008;180(5):2124–2128.Google Scholar
Tanrikut, C, Feldman, AS, Altemus, M, Paduch, DA, Schlegel, PN. Adverse effect of paroxetine on sperm. Fertil Steril. 2010;94(3):1021–1026.Google Scholar
Samplaski, MK, Lo, K, Grober, E, Jarvi, K. Finasteride use in the male infertility population: effects on semen and hormone parameters. Fertil Steril. 2013;100(6):1542–1546.Google Scholar
Sharma, R, Harlev, A, Agarwal, A, Esteves, SC. Cigarette smoking and semen quality: a new meta-analysis examining the effect of the 2010 World Health Organization Laboratory Methods for the Examination of Human Semen. Eur Urol. 2016;70(4):635–645.Google Scholar
Fraga, CG, Motchnik, PA, Wyrobek, AJ, Rempel, DM, Ames, BN. Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res. 1996;351(2):199–203.Google Scholar
Jenkins, TG, James, ER, Alonso, DF, et al. Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology. 2017;5(6):1089–1099.Google Scholar
Hammadeh, ME, Hamad, MF, Montenarh, M, Fischer-Hammadeh, C. Protamine contents and P1/P2 ratio in human spermatozoa from smokers and non-smokers. Hum Reprod. 2010;25(11):2708–2720.Google Scholar
Boeri, L, Capogrosso, P, Ventimiglia, E, et al. Heavy cigarette smoking and alcohol consumption are associated with impaired sperm parameters in primary infertile men. Asian J Androl. 2019;21(5):478–485.Google Scholar
Sailer, BL, Sarkar, LJ, Bjordahl, JA, Jost, LK, Evenson, DP. Effects of heat stress on mouse testicular cells and sperm chromatin structure. J Androl. 1997;18(3):294–301.Google Scholar
Thonneau, P, Bujan, L, Multigner, L, Mieusset, R. Occupational heat exposure and male fertility: a review. Hum Reprod. 1998;13(8):2122–2125.Google Scholar
Jurewicz, J, Dziewirska, E, Radwan, M, Hanke, W. Air pollution from natural and anthropic sources and male fertility. Reprod Biol Endocrinol. 2018;16(1):109.Google Scholar
Snijder, CA, te Velde, E, Roeleveld, N, Burdorf, A. Occupational exposure to chemical substances and time to pregnancy: a systematic review. Hum Reprod Update. 2012;18(3):284–300.Google Scholar
Spano, M, Bonde, JP, Hjollund, 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
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. 2020;244:8–15.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
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(11):e0165125.Google Scholar
Zini, A, Boman, J, Belzile, E, Ciampi, A. Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod. 2008;23:2663–2668.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(1):54–60.e3.Google Scholar
Gawecka, JE, Boaz, S, Kasperson, K, Nguyen, H, Evenson, DP, Ward, WS. Luminal fluid of epididymis and vas deferens contributes to sperm chromatin fragmentation. Hum Reprod. 2015;30(12):2725–2736.Google Scholar
Majzoub, A, Agarwal, A, Cho, CL, Esteves, SC. Sperm DNA fragmentation testing: a cross sectional survey on current practices of fertility specialists. Transl Androl Urol. 2017;6(Suppl. 4):S710–S719.Google Scholar
Practice Committee of the American Society for Reproductive Medicine. The clinical utility of sperm DNA integrity testing: a guideline. Fertil Steril. 2013;99(3):673–677.Google Scholar
Agarwal, A, Majzoub, A, Esteves, SC, Ko, E, Ramasamy, R, Zini, A. Clinical utility of sperm DNA fragmentation testing: practice recommendations based on clinical scenarios. Transl Androl Urol. 2016;5(6):935–950.Google Scholar
Kroese, ACJ, de Lange, NM, Collins, J, Evers, JLH. Surgery or embolization for varicoceles in subfertile men. Cochrane Database Syst Rev. 2012;10:CD000479.Google Scholar
Attia, AM, Abou-Setta, AM, Al-Inany, HG. Gonadotrophins for idiopathic male factor subfertility. Cochrane Database Syst Rev. 2013;23(8):CD005071.Google Scholar
Kamischke, A, Behre, HM, Bergmann, M, Simoni, M, Schäfer, T, Nieschlag, E. Recombinant human follicle stimulating hormone for treatment of male idiopathic infertility: a randomized, double-blind, placebo-controlled, clinical trial. Hum Reprod. 1998;13(3):596–603.Google Scholar
Santi, D, Spaggiari, G, Simoni, M. Sperm DNA fragmentation index as a promising predictive tool for male infertility diagnosis and treatment management: meta-analyses. Reprod Biomed Online. 2018;37(3):315–326.Google Scholar
Smits, RM, Mackenzie-Proctor, R, Yazdani, A, Stankiewicz, MT, Jordan, V, Showell, MG. Antioxidants for male subfertility. Cochrane Database Syst Rev. 2019;3(3):CD007411.Google Scholar
Hanson, BM, Aston, KI, Jenkins, TG, Carrell, DT, Hotaling, JM. The impact of ejaculatory abstinence on semen analysis parameters: a systematic review. J Assist Reprod Genet. 2018;35(2):213–220.Google Scholar
Ramos, L, De Boer, P, Meuleman, EJ, Braat, DD, Wetzels, AM. Evaluation of ICSI-selected epididymal sperm samples of obstructive azoospermic males by the CKIA system. J Androl. 2004;25(3):406–411.Google Scholar
Said, TM, Land, JA. Effects of advanced selection methods on sperm quality and ART outcome: a systematic review. Hum Reprod Update. 2011;17(6):719–733.Google Scholar
Strassburger, D, Friedler, S, Raziel, A, Schachter, M, Kasterstein, E, Ron-el, R. Very low sperm count affects the result of intracytoplasmic sperm injection. J Assist Reprod Genet. 2000;17(8):431–436.Google Scholar
Greco, E, Scarselli, F, Lacobelli, M, et al. Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod. 2005;20(1):226–230.Google Scholar
Esteves, SC, Roque, M, Bradley, CK, Garrido, N. Reproductive outcomes of testicular versus ejaculated sperm for intracytoplasmic sperm injection among men with high levels of DNA fragmentation in semen: systematic review and meta-analysis. Fertil Steril. 2017;108(3):456–467.Google Scholar

References

Baskaran, S, Finelli, R, Agarwal, A, Henkel, R. Diagnostic value of routine semen analysis in clinical andrology. Andrologia. 2020;12:e13614.Google Scholar
Eisenberg, ML, Li, S, Behr, B, Pera, RR, Cullen, MR. Relationship between semen production and medical comorbidity. Fertil Steril. 2015;103:66–71.Google Scholar
Wen, J, Jiang, J, Ding, C, et al. Birth defects in children conceived by in vitro fertilization and intracytoplasmic sperm injection: a meta-analysis. Fertil Steril. 2012;97(6):1331–1337.Google Scholar
Sakkas, D, Ramalingam, M, Garrido, N, Barratt, CL. Sperm selection in natural conception: what can we learn from Mother Nature to improve assisted reproduction outcomes? Hum Reprod Update. 2015;21:711–726.Google Scholar
Baldi, E, Tamburrino, L, Muratori, M, Degl’Innocenti, S, Marchiani, S. Adverse effects of in vitro manipulation of spermatozoa. Anim Reprod Sci. 2020;14:106314.Google Scholar
Davies, MJ, Moore, VM, Willson, KJ, et al. Reproductive technologies and the risk of birth defects. N Engl J Med. 2012;366:1803–1813.Google Scholar
Bonduelle, M, Wennerholm, UB, Loft, A, et al. A multi-centre cohort study of the physical health of 5-year-old children conceived after intracytoplasmic sperm injection, in vitro fertilization and natural conception. Hum Reprod. 2005;20:413–419.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
Baldi, E, Casano, R, Falsetti, C, Krausz, C, Maggi, M, Forti, G. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa. J Androl. 1991;12:323–330.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;11:1661–1667.Google Scholar
Baro Graf, C, Ritagliati, C, Torres-Monserrat, V, et al. Membrane potential assessment by fluorimetry as a predictor tool of human sperm fertilizing capacity. Front Cell Dev Biol. 2020;7:383.Google Scholar
Selvaraj, V, Buttke, DE, Asano, A, et al. GM1 dynamics as a marker for membrane changes associated with the process of capacitation in murine and bovine spermatozoa. J Androl. 2007;28:588–599.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;84:408–422.Google Scholar
Ostermeier, GC, Cardona, C, Moody, MA, et al. Timing of sperm capacitation varies reproducibly among men. Mol Reprod Dev. 2018;85:387–396.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;84:423–435.Google Scholar
Sharara, F, Seaman, E, Morris, R, et al. Multicentric, prospective observational data show sperm capacitation predicts male fertility, and cohort comparison reveals a high prevalence of impaired capacitation in men questioning their fertility. Reprod Biomed Online. 2020;41:69–79.Google Scholar
Mortimer, ST, van der Horst, G, Mortimer, D. The future of computer-aided sperm analysis. Asian J Androl. 2015;17:545–553.Google Scholar
Katz, DF, Overstreet, JW. Sperm motility assessment by videomicrography. Fertil Steril. 1981;35:188–193.Google Scholar
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;10:2928–2937.Google Scholar
Mortimer, D, Mortimer, ST. Computer-aided sperm analysis (CASA) of sperm motility and hyperactivation. Methods Mol Biol. 2013;927:77–87.Google Scholar
Senn, A, Germond, M, De Grandi, P. Immunofluorescence study of actin, acrosin, dynein, tubulin and hyaluronidase and their impact on in-vitro fertilization. Hum Reprod. 1992;7:841–849.Google Scholar
Sharma, R, Hogg, J, Bromham, DR. Is spermatozoan acrosin a predictor of fertilization and embryo quality in the human? Fertil Steril. 1993;60:881–887.Google Scholar
Menkveld, R, Rhemrev, JP, Franken, DR, Vermeiden, JP, Kruger, TF. Acrosomalmorphology as a novel criterion for male fertility diagnosis: relation with acrosin activity, morphology (strict criteria), and fertilization in vitro. Fertil Steril. 1996;65:637–644.Google Scholar
Yang, YS, Chen, SU, Ho, HN, et al. Acrosin activity of human sperm did not correlate with IVF. Arch Androl. 1994;32:13–19.Google Scholar
Liu, DY, Baker, HWG. Relationships between human sperm acrosin, acrosomes, morphology and fertilization in vitro. Hum Reprod. 1990;5:298–303.Google Scholar
Parinaud, J, Vieitez, G, Moutaffian, H, Richoilley, G, Labal, B. Variations in spontaneous and induced acrosome reaction: correlations with semen parameters and in-vitro fertilization results. Hum Reprod. 1995;10:2085–2089.Google Scholar
Xu, F, Guo, G, Zhu, W, Fan, L. Human sperm acrosome function assays are predictive of fertilization rate in vitro: a retrospective cohort study and meta-analysis. Reprod Biol Endocrinol. 2018;16:81.Google Scholar
Xu, F, Zhu, H, Zhu, W, Fan, L. Human sperm acrosomal status, acrosomal responsiveness, and acrosin are predictive of the outcomes of in vitro fertilization: a prospective cohort study. Reprod Biol. 2018;18:344–354.Google Scholar
Chen, X, Zheng, Y, Zheng, J, Lin, J, Zhang, L, Jin, J. The progesterone-induced sperm acrosome reaction is a good option for the prediction of fertilization in vitro compared with other sperm parameters. Andrologia. 2019;51:e13278.Google Scholar
Jin, M, Fujiwara, E, Kakiuchi, Y, et al. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci U S A. 2011;108:4892–4896.Google Scholar
Gahlay, GK, Rajput, N. The enigmatic sperm proteins in mammalian fertilization: an overview. Biol Reprod. 2020;103(6):1171–1185.Google Scholar
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;49:688–697.Google Scholar
Liu, DY, Baker, HW. High frequency of defective sperm–zona pellucida interaction in oligozoospermic infertile men. Hum Reprod. 2004;19:228–233.Google Scholar
Yao, YQ, Yeung, WS, Ho, PC. The factors affecting sperm binding to the zona pellucida in the hemizona binding assay. Hum Reprod. 1996;11:1516–1519.Google Scholar
Vogiatzi, P, Chrelias, C, Cahill, DJ, et al. Hemizona assay and sperm penetration assay in the prediction of IVF outcome: a systematic review. Biomed Res Int. 2013;2013:945825.Google Scholar
Oehninger, S, Franken, DR, Sayed, EM, Barroso, G, Kohm, P. Sperm function assays and their predictive value for fertilization outcome in IVF therapy: a meta analysis. Hum Reprod Update. 2000;6:1160–1168.Google Scholar
Aydin, H, Sultana, A, Li, S, Thavalingam, A, Lee, JE. Molecular architecture of the human sperm IZUMO1 and egg JUNO fertilization complex. Nature. 2016;534:562–565.Google Scholar
Granados-Gonzalez, V, Aknin-Seifer, I, Touraine, RL, Chouteau, J, Wolf, JP, Levy, R. Preliminary study on the role of the human IZUMO gene in oocyte-spermatozoa fusion failure. Fertil Steril. 2008;90:1246–1248.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;15:471–476.Google Scholar
Ford, WC, Williams, KM, Harrison, S, et al. Value of the hamster oocyte test and computerised measurements of sperm motility in predicting if four or more viable embryos will be obtained in an IVF cycle. Int J Androl. 2001;24:109–119.Google Scholar
Ho, LM, Lim, AS, Lim, TH, Hum, SC, Yu, SL, Kruger, TF. Correlation between semen parameters and the Hamster Egg Penetration Test (HEPT) among fertile and subfertile men in Singapore. J Androl. 2007;28:158–163.Google Scholar
Simon, L, Murphy, K, Shamsi, MB, et al. Paternal influence of sperm DNA integrity on early embryonic development. Hum Reprod. 2014;29:2402e12.Google Scholar
Zini, A, Boman, JM, Belzile, E, et al. Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod. 2008;23:2663e8.Google Scholar
Dutta, S, Henkel, R, Agarwal, A. Comparative analysis of tests used to assess sperm chromatin integrity and DNA fragmentation. Andrologia. 2020; 6:e13718.Google Scholar
Marchiani, S, Tamburrino, L, Muratori, M, Baldi, E. Spermatozoal chromatin structure: role in sperm functions and fertilization. In: Arafa, M, Elbardisi, H, Majzoub, A, Agarwal, A. eds. Genetics of Male Infertility: A Case-Based Guide for Clinicians. Springer; 2020:39–57.Google Scholar
Marchiani, S, Tamburrino, L, Benini, F, et al. Chromatin protamination and CATSPER expression in spermatozoa predict clinical outcomes after assisted reproduction programs. Sci Rep. 2017;7:15122.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
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
World Health Organization. Laboratory Manual for the Examination and Processing of Human Semen. 5th ed. WHO Press; 2010.Google Scholar

References

Lehtonen, J, Parker, GA. Gamete competition, gamete limitation, and the evolution of the two sexes. Mol Hum Reprod. 2014;20(12):1161–1168.Google Scholar
Nascimento, JM, Shi, LZ, Meyers, S, et al. The use of optical tweezers to study sperm competition and motility in primates. J R Soc Interface. 2008;5(20):297–302.Google Scholar
Sakkas, D, Ramalingam, M, Garrido, N, Barratt, CL. Sperm selection in natural conception: what can we learn from Mother Nature to improve assisted reproduction outcomes? Hum Reprod Update. 2015;21(6):711–726.Google Scholar
Katz, DF, Drobnis, EZ, Overstreet, JW. Factors regulating mammalian sperm migration through the female reproductive tract and oocyte vestments. Gamete Res. 1989;22(4):443–469.Google Scholar
Wolf, DP, Blasco, L, Khan, MA, Litt, M. Human cervical mucus. IV. Viscoelasticity and sperm penetrability during the ovulatory menstrual cycle. Fertil Steril. 1978;30(2):163–169.Google Scholar
Khandwala, YS, Baker, VL, Shaw, GM, Stevenson, DK, Lu, Y, Eisenberg, ML. Association of paternal age with perinatal outcomes between 2007 and 2016 in the United States: population based cohort study. BMJ. 2018;363:k4372.Google Scholar
Evenson, DP, Darzynkiewicz, Z, Melamed, MR. Relation of mammalian sperm chromatin heterogeneity to fertility. Science. 1980;210(4474):1131–1133.Google Scholar
Evenson, D, Darzynkiewicz, Z, Jost, L, Janca, F, Ballachey, B. Changes in accessibility of DNA to various fluorochromes during spermatogenesis. Cytometry. 1986;7(1):45–53.Google Scholar
Bianchi, PG, Manicardi, GC, Bizzaro, D, Bianchi, U, Sakkas, D. Effect of deoxyribonucleic acid protamination on fluorochrome staining and in situ nick-translation of murine and human mature spermatozoa. Biol Reprod. 1993;49(5):1083–1088.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(8):613–619.Google Scholar
Sakkas, D, Seli, E, Manicardi, GC, Nijs, M, Ombelet, W, Bizzaro, D. The presence of abnormal spermatozoa in the ejaculate: did apoptosis fail? Hum Fertil (Camb). 2004;7(2):99–103.Google Scholar
Oehninger, S, Morshedi, M, Weng, SL, Taylor, S, Duran, H, Beebe, S. Presence and significance of somatic cell apoptosis markers in human ejaculated spermatozoa. Reprod Biomed Online. 2003;7(4):469–476.Google Scholar
Jodar, M, Selvaraju, S, Sendler, E, Diamond, MP, Krawetz, SA. The presence, role and clinical use of spermatozoal RNAs. Hum Reprod Update. 2013;19(6):604–624.Google Scholar
Cayli, S, Jakab, A, Ovari, L, et al. Biochemical markers of sperm function: male fertility and sperm selection for ICSI. Reprod Biomed Online. 2003;7(4):462–468.Google Scholar
Yagci, A, Murk, W, Stronk, J, Huszar, G. Spermatozoa bound to solid state hyaluronic acid show chromatin structure with high DNA chain integrity: an acridine orange fluorescence study. J Androl. 2010;31(6):566–572.Google Scholar
Burl, RB, Clough, S, Sendler, E, Estill, M, Krawetz, SA. Sperm RNA elements as markers of health. Syst Biol Reprod Med. 2018;64(1):25–38.Google Scholar
Manicardi, GC, Tombacco, A, Bizzaro, D, Bianchi, U, Bianchi, PG, Sakkas, D. DNA strand breaks in ejaculated human spermatozoa: comparison of susceptibility to the nick translation and terminal transferase assays. Histochem J. 1998;30(1):33–39.Google Scholar
Manicardi, GC, Bianchi, PG, Pantano, S, et al. Presence of endogenous nicks in DNA of ejaculated human spermatozoa and its relationship to chromomycin A3 accessibility. Biol Reprod. 1995;52(4):864–867.Google Scholar
Varghese, AC, Bragais, FM, Mukhopadhyay, D, et al. Human sperm DNA integrity in normal and abnormal semen samples and its correlation with sperm characteristics. Andrologia. 2009;41(4):207–215.Google Scholar
Aitken, RJ, De Iuliis, GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2010;16(1):3–13.Google Scholar
Sakkas, D, Seli, E, Bizzaro, D, Tarozzi, N, Manicardi, GC. Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. Reprod Biomed Online. 2003;7(4):428–432.Google Scholar
Said, TM, Agarwal, A, Zborowski, M, Grunewald, S, Glander, HJ, Paasch, U. Utility of magnetic cell separation as a molecular sperm preparation technique. J Androl. 2008;29(2):134–142.Google Scholar
Lee, TH, Liu, CH, Shih, YT, et al. Magnetic-activated cell sorting for sperm preparation reduces spermatozoa with apoptotic markers and improves the acrosome reaction in couples with unexplained infertility. Hum Reprod. 2010;25(4):839–846.Google Scholar
Lepine, S, McDowell, S, Searle, LM, Kroon, B, Glujovsky, D, Yazdani, A. Advanced sperm selection techniques for assisted reproduction. Cochrane Database Syst Rev. 2019;7(7):CD010461.Google Scholar
Jakab, A, Sakkas, D, Delpiano, E, et al. Intracytoplasmic sperm injection: a novel selection method for sperm with normal frequency of chromosomal aneuploidies. Fertil Steril. 2005;84(6):1665–1673.Google Scholar
Sati, L, Huszar, G. Methodology of aniline blue staining of chromatin and the assessment of the associated nuclear and cytoplasmic attributes in human sperm. Methods Mol Biol. 2013;927:425–436.Google Scholar
Huszar, G, Ozkavukcu, S, Jakab, A, Celik-Ozenci, C, Sati, GL, Cayli, S. Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: selection of sperm for intracytoplasmic sperm injection. Curr Opin Obstet Gynecol. 2006;18(3):260–267.Google Scholar
Ovári, L, Sati, L, Stronk, J, Borsos, A, Ward, DC, Huszar, G. Double probing individual human spermatozoa: aniline blue staining for persistent histones and fluorescence in situ hybridization for aneuploidies. Fertil Steril. 2010;93(7):2255–2261.Google Scholar
Worrilow, KC, Eid, S, Woodhouse, D, et al. Use of hyaluronan in the selection of sperm for intracytoplasmic sperm injection (ICSI): significant improvement in clinical outcomes – multicenter, double-blinded and randomized controlled trial. Hum Reprod. 2013;28(2):306–314.Google Scholar
Miller, D, Pavitt, S, Sharma, V, et al. Physiological, hyaluronan-selected intracytoplasmic sperm injection for infertility treatment (HABSelect): a parallel, two-group, randomised trial. Lancet. 2019;393(10170):416–422.Google Scholar
Tarozzi, N, Nadalini, M, Bizzaro, D, et al. Sperm-hyaluronan-binding assay: clinical value in conventional IVF under Italian law. Reprod Biomed Online. 2009;19(Suppl. 3):35–43.Google Scholar
Parmegiani, L, Cognigni, GE, Bernardi, S, et al. Comparison of two ready-to-use systems designed for sperm-hyaluronic acid binding selection before intracytoplasmic sperm injection: PICSI vs. Sperm Slow: a prospective, randomized trial. Fertil Steril. 2012;98(3):632–637.Google Scholar
Majumdar, G, Majumdar, A. A prospective randomized study to evaluate the effect of hyaluronic acid sperm selection on the intracytoplasmic sperm injection outcome of patients with unexplained infertility having normal semen parameters. J Assist Reprod Genet. 2013;30(11):1471–1475.Google Scholar
McDowell, S, Kroon, B, Ford, E, Hook, Y, Glujovsky, D, Yazdani, A. Advanced sperm selection techniques for assisted reproduction. Cochrane Database Syst Rev. 2014(10):CD010461.Google Scholar
Hasanen, E, Elqusi, K, ElTanbouly, S, et al. PICSI vs. MACS for abnormal sperm DNA fragmentation ICSI cases: a prospective randomized trial. J Assist Reprod Genet. 2020;37(10):2605–2613.Google Scholar
Schuster, TG, Cho, B, Keller, LM, Takayama, S, Smith, GD. Isolation of motile spermatozoa from semen samples using microfluidics. Reprod Biomed Online. 2003;7(1):75–81.Google Scholar
Smith, GD, Takayama, S. Application of microfluidic technologies to human assisted reproduction. Mol Hum Reprod. 2017;23(4):257–268.Google Scholar
Riordon, J, Tarlan, F, You, JB, et al. Two-dimensional planar swimming selects for high DNA integrity sperm. Lab Chip. 2019;19(13):2161–2167.Google Scholar
Quinn, MM, Jalalian, L, Ribeiro, S, et al. Microfluidic sorting selects sperm for clinical use with reduced DNA damage compared to density gradient centrifugation with swim-up in split semen samples. Hum Reprod. 2018;33(8):1388–1393.Google Scholar
Shirota, K, Yotsumoto, F, Itoh, H, et al. Separation efficiency of a microfluidic sperm sorter to minimize sperm DNA damage. Fertil Steril. 2016;105(2):315–321 e1.Google Scholar
Gode, F, Gürbüz, AS, Tamer, B, Pala, I, Isik, AZ. The effects of microfluidic sperm sorting, density gradient and swim-up methods on semen oxidation reduction potential. Urol J. 2020;17(4):397–401.Google Scholar
Yildiz, K, Yuksel, S. Use of microfluidic sperm extraction chips as an alternative method in patients with recurrent in vitro fertilisation failure. J Assist Reprod Genet. 2019;36(7):1423–1429.Google Scholar
Parrella, A, Keating, D, Cheung, S, et al. A treatment approach for couples with disrupted sperm DNA integrity and recurrent ART failure. J Assist Reprod Genet. 2019;36(10):2057–2066.Google Scholar
Parrella, A, Tavares, RS, Haddad, M, et al. A novel method to attenuate embryo aneuploidy due to paternal inheritance. Fertil Steril. 2020;114(3):e424–e425.Google Scholar
Chan, PJ, Jacobson, JD, Corselli, JU, Patton, WC. A simple zeta method for sperm selection based on membrane charge. Fertil Steril. 2006;85(2):481–486.Google Scholar
Kheirollahi-Kouhestani, M, Razavi, S, Tavalaee, M, et al. Selection of sperm based on combined density gradient and Zeta method may improve ICSI outcome. Hum Reprod. 2009;24(10):2409–2416.Google Scholar
Simon, L, Ge, SQ, Carrell, DT. Sperm selection based on electrostatic charge. Methods Mol Biol. 2013;927:269–278.Google Scholar
Ainsworth, C, Nixon, B, Aitken, RJ. Development of a novel electrophoretic system for the isolation of human spermatozoa. Hum Reprod. 2005;20(8):2261–2270.Google Scholar
Ainsworth, C, Nixon, B, Jansen, RP, Aitken, RJ. First recorded pregnancy and normal birth after ICSI using electrophoretically isolated spermatozoa. Hum Reprod. 2007;22(1):197–220.Google Scholar
Fleming, SD, Ilad, RS, Griffin, AM, et al. Prospective controlled trial of an electrophoretic method of sperm preparation for assisted reproduction: comparison with density gradient centrifugation. Hum Reprod. 2008;23(12):2646–2651.Google Scholar
Tran, D, Cooke, S, Illingworth, PJ, Gardner, DK. Deep learning as a predictive tool for fetal heart pregnancy following time-lapse incubation and blastocyst transfer. Hum Reprod. 2019;34(6):1011–1018.Google Scholar
Zaninovic, N, Rosenwaks, Z. Artificial intelligence in human in vitro fertilization and embryology. Fertil Steril. 2020;114(5):914–920.Google Scholar
Butola, A, Popova, D, Prasad, DK, et al. High spatially sensitive quantitative phase imaging assisted with deep neural network for classification of human spermatozoa under stressed condition. Sci Rep. 2020;10(1):13118.Google Scholar
Kandel, ME, Rubessa, M, He, YR, et al. Reproductive outcomes predicted by phase imaging with computational specificity of spermatozoon ultrastructure. Proc Natl Acad Sci U S A. 2020;117(31):18302–18309.Google Scholar
Kovac, JR, Smith, RP, Cajipe, M, Lamb, DJ, Lipshultz, LI. Men with a complete absence of normal sperm morphology exhibit high rates of success without assisted reproduction. Asian J Androl. 2017;19(1):39–42.Google Scholar
Bartoov, B, Berkovitz, A, Eltes, F. Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. N Engl J Med. 2001;345(14):1067–1068.Google Scholar
Antinori, M, Licata, E, Dani, G, et al. Intracytoplasmic morphologically selected sperm injection: a prospective randomized trial. Reprod Biomed Online. 2008;16(6):835–841.Google Scholar
Setti, SA, Ferreira, RC, Braga, DPAF, Figueira, RCS, Iaconelli, A Jr, Borges, E Jr. Intracytoplasmic sperm injection outcome versus intracytoplasmic morphologically selected sperm injection outcome: a meta-analysis. Reprod Biomed Online. 2010;21(4):450–455.Google Scholar
Teixeira, DM, Hadyme Miyague, A, Barbosa, MA, et al. Regular (ICSI) versus ultra-high magnification (IMSI) sperm selection for assisted reproduction. Cochrane Database Syst Rev. 2020;2(2):CD010167.Google Scholar
Mallidis, C, Sanchez, V, Wistuba, J, et al. Raman microspectroscopy: shining a new light on reproductive medicine. Hum Reprod Update. 2014;20(3):403–414.Google Scholar
Huser, T, Orme, CA, Hollars, CW, Corzett, MH, Balhorn, R. Raman spectroscopy of DNA packaging in individual human sperm cells distinguishes normal from abnormal cells. J Biophotonics. 2009;2(5):322–332.Google Scholar
Da Costa, R, Amaral, S, Redmann, K, Kliesch, S, Schlatt, S. Spectral features of nuclear DNA in human sperm assessed by Raman microspectroscopy: effects of UV-irradiation and hydration. PLoS ONE. 2018;13(11):e0207786.Google Scholar
De Angelis, A, Ferrara, MA, Coppola, G, et al. Combined Raman and polarization sensitive holographic imaging for a multimodal label-free assessment of human sperm function. Sci Rep. 2019;9(1):4823.Google Scholar
Sakkas, D, Alvarez, JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010;93(4):1027–1036.Google Scholar
Esteves, SC, Sánchez-Martín, F, Sánchez-Martín, P, Schneider, DT, Gosálvez, J. Comparison of reproductive outcome in oligozoospermic men with high sperm DNA fragmentation undergoing intracytoplasmic sperm injection with ejaculated and testicular sperm. Fertil Steril. 2015;104(6):1398–1405.Google Scholar
Awaga, HA, Bosdou, JK, Goulis, DG, et al. Testicular versus ejaculated spermatozoa for ICSI in patients without azoospermia: a systematic review. Reprod Biomed Online. 2018;37(5):573–580.Google Scholar
Gosálvez, J, González-Martínez, M, López-Fernández, C, Fernández, JL, Sánchez-Martín, P. Shorter abstinence decreases sperm deoxyribonucleic acid fragmentation in ejaculate. Fertil Steril. 2011;96(5):1083–1086.Google Scholar
Scarselli, F, Casciani, V, Cursio, E, et al. Influence of human sperm origin, testicular or ejaculated, on embryo morphokinetic development. Andrologia. 2018;50(8):e13061.Google Scholar
Vaughan, DA, Sakkas, D. Sperm selection methods in the 21st century. Biol Reprod. 2019;101(6):1076–1082.Google Scholar
Albertini, DF. The problem with being choosy when it comes to sperm selection. J Assist Reprod Genet. 2019;36(7):1297–1298.Google Scholar
Henkel, R. Sperm preparation: state-of-the-art physiological aspects and application of advanced sperm preparation methods. Asian J Androl. 2012;14(2):260–269.Google Scholar

References

World Health Organization, ed. WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th ed. World Health Organization; 2010.Google Scholar
Henkel, RR, Schill, W-B. Sperm preparation for ART. Reprod Biol Endocrinol. 2003;1(1):108.Google Scholar
Dai, X, Wang, Y, Cao, F, et al. Sperm enrichment from poor semen samples by double density gradient centrifugation in combination with swim-up for IVF cycles. Sci Rep. 2020;10(1):2286.Google Scholar
Oguz, Y, Guler, I, Erdem, A, et al. The effect of swim-up and gradient sperm preparation techniques on deoxyribonucleic acid (DNA) fragmentation in subfertile patients. J Assist Reprod Genet. 2018;35(6):1083–1089.Google Scholar
Chen, Q, Zhao, J-Y, Xue, X, Zhu, G-X. The association between sperm DNA fragmentation and reproductive outcomes following intrauterine insemination, a meta analysis. Reprod Toxicol Elmsford N. 2019;86:50–55.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. 2020;244:8–15.Google Scholar
Boomsma, CM, Heineman, MJ, Cohlen, BJ, Farquhar, C. Semen preparation techniques for intrauterine insemination. Cochrane Database Syst Rev. 2007;4:CD004507.Google Scholar
Huszar, G, Ozkavukcu, S, Jakab, A, Celik-Ozenci, C, Sati, GL, Cayli, S. Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: selection of sperm for intracytoplasmic sperm injection: Curr Opin Obstet Gynecol. 2006;18(3):260–267.Google Scholar
Miller, D, Pavitt, S, Sharma, V, et al. Physiological, hyaluronan-selected intracytoplasmic sperm injection for infertility treatment (HABSelect): a parallel, two-group, randomised trial. Lancet. 2019;393(10170):416–422.Google Scholar
Lepine, S, McDowell, S, Searle, LM, Kroon, B, Glujovsky, D, Yazdani, A. Advanced sperm selection techniques for assisted reproduction. Cochrane Database Syst Rev. 2019;7:CD010461.Google Scholar
Gil, M, Sar-Shalom, V, Melendez Sivira, Y, Carreras, R, Checa, MA. Sperm selection using magnetic activated cell sorting (MACS) in assisted reproduction: a systematic review and meta-analysis. J Assist Reprod Genet. 2013;30(4):479–485.Google Scholar
Romany, L, Garrido, N, Motato, Y, Aparicio, B, Remohí, J, Meseguer, M. Removal of annexin V-positive sperm cells for intracytoplasmic sperm injection in ovum donation cycles does not improve reproductive outcome: a controlled and randomized trial in unselected males. Fertil Steril. 2014;102(6):1567–1575.Google Scholar
Chan, PJ, Jacobson, JD, Corselli, JU, Patton, WC. A simple zeta method for sperm selection based on membrane charge. Fertil Steril. 2006;85(2):481–486.Google Scholar
Nasr Esfahani, MH, Deemeh, MR, Tavalaee, M, Sekhavati, MH, Gourabi, H. Zeta sperm selection improves pregnancy rate and alters sex ratio in male factor infertility patients: a double-blind, randomized clinical trial. Int J Fertil Steril. 2016;10(2):253–260.Google Scholar
Karimi, N, Mohseni Kouchesfahani, H, Nasr-Esfahani, MH, Tavalaee, M, Shahverdi, A, Choobineh, H. DGC/zeta as a new strategy to improve clinical outcome in male factor infertility patients following intracytoplasmic sperm injection: a randomized, single-blind, clinical trial. Cell J. 2020;22(1):55–59.Google Scholar
Ainsworth, C, Nixon, B, Aitken, RJ. Development of a novel electrophoretic system for the isolation of human spermatozoa. Hum Reprod. 2005;20(8):2261–2270.Google Scholar
Fleming, SD, Ilad, RS, Griffin, A-MG, et al. Prospective controlled trial of an electrophoretic method of sperm preparation for assisted reproduction: comparison with density gradient centrifugation. Hum Reprod. 2008;23(12):2646–2651.Google Scholar
Duran-Retamal, M, Morris, G, Achilli, C, et al. Live birth and miscarriage rate following intracytoplasmic morphologically selected sperm injection vs intracytoplasmic sperm injection: an updated systematic review and meta-analysis. Acta Obstet Gynecol Scand. 2020;99(1):24–33.Google Scholar
Teixeira, DM, Miyague, AH, Barbosa, MA, et al. Regular (ICSI) versus ultra-high magnification (IMSI) sperm selection for assisted reproduction. Cochrane Database Syst Rev. 2020;2:CD010167.Google Scholar
Gianaroli, L, Magli, MC, Ferraretti, AP, et al. Birefringence characteristics in sperm heads allow for the selection of reacted spermatozoa for intracytoplasmic sperm injection. Fertil Steril. 2010;93(3):807–813.Google Scholar
Vermey, BG, Chapman, MG, Cooke, S, Kilani, S. The relationship between sperm head retardance using polarized light microscopy and clinical outcomes. Reprod Biomed Online. 2015;30(1):67–73.Google Scholar
Nosrati, R, Graham, PJ, Zhang, B, et al. Microfluidics for sperm analysis and selection. Nat Rev Urol. 2017;14(12):707–730.Google Scholar
Marzano, G, Chiriacò, MS, Primiceri, E, et al. Sperm selection in assisted reproduction: a review of established methods and cutting-edge possibilities. Biotechnol Adv. 2020;40:107498.Google Scholar
Samuel, R, Son, J, Jenkins, TG, et al. Microfluidic system for rapid isolation of sperm from microdissection TESE specimens. Urology. 2020;140:70–76.Google Scholar
Wang, R, Pan, W, Jin, L, et al. Artificial intelligence in reproductive medicine. Reproduction. 2019;158(4):139–154.Google Scholar
Dai, C, Zhang, Z, Huang, J, et al. Automated non-invasive measurement of single sperm’s motility and morphology. IEEE Trans Med Imaging. 2018;37(10):2257–2265.Google Scholar
Zhang, Z, Dai, C, Huang, J, et al. Robotic immobilization of motile sperm for clinical intracytoplasmic sperm injection. IEEE Trans Biomed Eng. 2019;66(2):444–452.Google Scholar
Practice Committee of the American Society for Reproductive Medicine in collaboration with the Society for Male Reproduction and Urology. The management of obstructive azoospermia: a committee opinion. Fertil Steril. 2019;111(5):873–880.Google Scholar
Shih, K-W, Shen, P-Y, Wu, C-C, Kang, Y-N. Testicular versus percutaneous epididymal sperm aspiration for patients with obstructive azoospermia: a systematic review and meta-analysis. Transl Androl Urol. 2019;8(6):631–640.Google Scholar
Practice Committee of the American Society for Reproductive Medicine. Management of nonobstructive azoospermia: a committee opinion. Fertil Steril. 2018;110(7):1239–1245.Google Scholar
Bernie, AM, Mata, DA, Ramasamy, R, Schlegel, PN. Comparison of microdissection testicular sperm extraction, conventional testicular sperm extraction, and testicular sperm aspiration for nonobstructive azoospermia: a systematic review and meta-analysis. Fertil Steril. 2015;104(5):1099–1103.Google Scholar
Deruyver, Y, Vanderschueren, D, Van der Aa, F. Outcome of microdissection TESE compared with conventional TESE in non-obstructive azoospermia: a systematic review. Andrology. 2014;2(1):20–24.Google Scholar
Flannigan, RK, Schlegel, PN. Microdissection testicular sperm extraction: preoperative patient optimization, surgical technique, and tissue processing. Fertil Steril. 2019;111(3):420–426.Google Scholar
Corona, G, Minhas, S, Giwercman, A, et al. Sperm recovery and ICSI outcomes in men with non-obstructive azoospermia: a systematic review and meta-analysis. Hum Reprod Update. 2019;25(6):733–757.Google Scholar
Ohlander, S, Hotaling, J, Kirshenbaum, E, Niederberger, C, Eisenberg, ML. Impact of fresh versus cryopreserved testicular sperm upon intracytoplasmic sperm injection pregnancy outcomes in men with azoospermia due to spermatogenic dysfunction: a meta-analysis. Fertil Steril. 2014;101(2):344–349.Google Scholar
Yu, Z, Wei, Z, Yang, J, et al. Comparison of intracytoplasmic sperm injection outcome with fresh versus frozen-thawed testicular sperm in men with nonobstructive azoospermia: a systematic review and meta-analysis. J Assist Reprod Genet. 2018;35(7):1247–1257.Google Scholar
Popal, W, Nagy, ZP. Laboratory processing and intracytoplasmic sperm injection using epididymal and testicular spermatozoa: what can be done to improve outcomes? Clin Sao Paulo Braz. 2013;68(Suppl. 1):125–130.Google Scholar
Baukloh, V, German Society for Human Reproductive Biology. Retrospective multicentre study on mechanical and enzymatic preparation of fresh and cryopreserved testicular biopsies. Hum Reprod. 2002;17(7):1788–1794.Google Scholar
Kovacic, B, Vlaisavljevic, V, Reljic, M. Clinical use of pentoxifylline for activation of immotile testicular sperm before ICSI in patients with azoospermia. J Androl. 2006;27(1):45–52.Google Scholar
Ebner, T, Tews, G, Mayer, RB, et al. Pharmacological stimulation of sperm motility in frozen and thawed testicular sperm using the dimethylxanthine theophylline. Fertil Steril. 2011;96(6):1331–1336.Google Scholar
Sallam, HN, Farrag, A, Agameya, A-F, El-Garem, Y, Ezzeldin, F. The use of the modified hypo-osmotic swelling test for the selection of immotile testicular spermatozoa in patients treated with ICSI: a randomized controlled study. Hum Reprod. 2005;20(12):3435–3440.Google Scholar
Nordhoff, V, Schüring, AN, Krallmann, C, et al. Optimizing TESE-ICSI by laser-assisted selection of immotile spermatozoa and polarization microscopy for selection of oocytes. Andrology. 2013;1(1):67–74.Google Scholar
Rubino, P, Viganò, P, Luddi, A, Piomboni, P. The ICSI procedure from past to future: a systematic review of the more controversial aspects. Hum Reprod Update. 2015; 22(2):194–227.Google Scholar
Mangum, CL, Patel, DP, Jafek, AR, et al. Towards a better testicular sperm extraction: novel sperm sorting technologies for non-motile sperm extracted by microdissection TESE. Transl Androl Urol. 2020;9(2):S206–S214.Google Scholar
Esteves, SC, Roque, M, Bradley, CK, Garrido, N. Reproductive outcomes of testicular versus ejaculated sperm for intracytoplasmic sperm injection among men with high levels of DNA fragmentation in semen: systematic review and meta-analysis. Fertil Steril. 2017;108(3):456–467.Google Scholar
Ambar, RF, Agarwal, A, Majzoub, A, et al. The use of testicular sperm for intracytoplasmic sperm injection in patients with high sperm DNA damage: a systematic review. World J Mens Health. 2020;200084.Google Scholar
Awaga, HA, Bosdou, JK, Goulis, DG, et al. Testicular versus ejaculated spermatozoa for ICSI in patients without azoospermia: a systematic review. Reprod Biomed Online. 2018;37(5):573–580.Google Scholar
Kang, Y-N, Hsiao, Y-W, Chen, C-Y, Wu, C-C. Testicular sperm is superior to ejaculated sperm for ICSI in cryptozoospermia: an update systematic review and meta-analysis. Sci Rep. 2018;8(1):7874.Google Scholar
Ku, F-Y, Wu, C-C, Hsiao, Y-W, Kang, Y-N. Association of sperm source with miscarriage and take-home baby after ICSI in cryptozoospermia: a meta-analysis of testicular and ejaculated sperm. Andrology. 2018;6(6):882–889.Google Scholar

References

Agarwal, A, Mulgund, A, Hamada, A, Chyatte, MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 2015;13:37.Google Scholar
Jarow, JP, Sharlip, ID, Belker, AM, et al. Best practice policies for male infertility. J Urol. 2002;77(5):873–882.Google Scholar
World Health Organization. Laboratory Manual for the Examination and Processing of Human Semen. Cambridge University Press; 2010.Google Scholar
Gudeloglu, A, Parekattil, SJ. Update in the evaluation of the azoospermic male. Clinics (Sao Paolo). 2013;68(Suppl. 1):27–34.Google Scholar
Esteves, SC. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl. 2015;17(3):459–470.Google Scholar
Silber, SJ. Microsurgical TESE and the distribution of spermatogenesis in non-obstructive azoospermia. Hum Reprod. 2000;15(11):2278–2784.Google Scholar
Craft, I, Tsirigotis, M, Bennett, V, et al. Percutaneous epididymal sperm aspiration and intracytoplasmic sperm injection in the management of infertility due to obstructive azoospermia. Fertil Steril. 1995;63(5):1038–1042.Google Scholar
Donat, R, Mcneill, AS, Fitzpatrick, DR, Hargreave, TB. The incidence of cystic fibrosis gene mutations in patients with congenital bilateral absence of the vas deferens in Scotland. Br J Urol. 1997;79(1):74–77.Google Scholar
Grangeia, A, Niel, F, Carvalho, F, et al. Characterization of cystic fibrosis conductance transmembrane regulator gene mutations and IVS8 poly (T) variants in Portuguese patients with congenital absence of the vas deferens. Hum Reprod. 2004;19(11):2502–2508.Google Scholar
Tournaye, H. Update on surgical sperm recovery: the European view. Hum Fertil. 2010;13(4):242–246.Google Scholar
Vloeberghs, V, Verheyen, G, Haentjens, P, Goossens, A, Polyzos, NP, Tournaye, H. How successful is TESE-ICSI in couples with non-obstructive azoospermia? Hum Reprod. 2015;30(8):1790–1796.Google Scholar
Shah, R, Gupta, C. Advances in sperm retrieval techniques in azoospermic men: a systematic review. Arab J Urol. 2018;16(1):125–131.Google Scholar
Flannigan, RK, Schlegel, PN. Microdissection testicular sperm extraction: preoperative patient optimization, surgical technique, and tissue processing. Fertil Steril. 2019;111(3):420–426.Google Scholar
Turek, PJ, Cha, I, Ljung, BM. Systematic fine-needle aspiration of the testis: correlation to biopsy and results of organ “mapping” for mature sperm in azoospermic men. Urology. 1997;49(5):743–748.Google Scholar
Caroppo, E, Colpi, EM, Gazzano, G, et al. The seminiferous tubule caliber pattern as evaluated at high magnification during microdissection testicular sperm extraction predicts sperm retrieval in patients with non-obstructive azoospermia. Andrology. 2019;7(1):8–14.Google Scholar
Deruyver, Y, Vanderschueren, D, Van der Aa, F. Outcome of microdissection TESE compared with conventional TESE in non-obstructive azoospermia: a systematic review. Andrology. 2014;2(1):20–24.Google Scholar
Samuel, R, Badamjav, O, Murphy, KE, et al. Microfluidics: the future of microdissection TESE? Syst Biol Reprod Med. 2016;62(3):161–170.Google Scholar
Peterson, CM, Hammoud, AO, Lindley, E, Carrell, DT, Wilson, K. Assisted reproductive technology practice management. In: Carrell, D, Peterson, CM, eds. Reproductive Endocrinology and Infertility: Integrating Modern Clinical and Laboratory Practice. Springer; 2010:7–37.Google Scholar
Parmegiani, L, Cognigni, GE, Bernardi, S, et al. Comparison of two ready-to-use systems designed for sperm-hyaluronic acid binding selection before intracytoplasmic sperm injection: PICSI vs. Sperm Slow: a prospective, randomized trial. Fertil Steril. 2012;98(3):632–637.Google Scholar
Samuel, R, Feng, H, Jafek, A, Despain, D, Jenkins, T, Gale, B. Microfluidic-based sperm sorting & analysis for treatment of male infertility. Transl Androl Urol. 2018;7(Suppl. 3):S336–S347.Google Scholar
Esteves, SC, Varghese, AC. Laboratory handling of epididymal and testicular spermatozoa: what can be done to improve sperm injections outcome. J Hum Reprod Sci. 2012;5(3):233–243.Google Scholar
Popal, W, Nagy, ZP. Laboratory processing and intracytoplasmic sperm injection using epididymal and testicular spermatozoa: what can be done to improve outcomes? Clinics (Sao Paolo). 2013;68(Suppl. 1):125–130.Google Scholar
Ramasamy, R, Schlegel, PN. Microdissection testicular sperm extraction: effect of prior biopsy on success of sperm retrieval. J Urol. 2007;177(4):1447–1449.Google Scholar
Feng, X, Liu, L, Yu, BQ, Huang, JM, Gu, LD, Xu, DF. Effect of optimized collagenase digestion on isolated and cultured nucleus pulposus cells in degenerated intervertebral discs. Medicine (Baltimore). 2018;97(44):e12977.Google Scholar
Ghasemzadeh, A, Karkon-Shayan, F, Yousefzadeh, S, Naghavi-Behzad, M, Hamdi, K. Study of pentoxifylline effects on motility and viability of spermatozoa from infertile asthenozoospermic males. Niger Med J. 2016;57(6):324–328.Google Scholar
Baukloh, V. Retrospective multicentre study on mechanical and enzymatic preparation of fresh and cryopreserved testicular biopsies. Hum Reprod. 2002;17(7):1788–1794.Google Scholar
Sackmann, EK, Fulton, AL, Beebe, DJ. The present and future role of microfluidics in biomedical research. Nature. 2014;507(7491):181–189.Google Scholar
Swain, JE, Lai, D, Takayama, S, Smith, GD. Thinking big by thinking small: application of microfluidic technology to improve ART. Lab Chip. 2013;13(7):1213–1224.Google Scholar
Xia, Y, Whitesides, GM. Soft lithography. Angew Chem Int Ed Eng. 1998;37(5):550–575.Google Scholar
Vaughan, DA, Sakkas, D, Gardner, DK. Sperm selection methods in the 21st century. Biol Reprod. 2019;101(6):1076–1082.Google Scholar
Beebe, DJ, Mensing, GA, Walker, GM. Physics and applications of microfluidics in biology. Annu Rev Biomed Eng. 2002;4:261–286.Google Scholar
Brody, JP, Yager, P, Goldstein, RE, Austin, RH. Biotechnology at low Reynolds numbers. Biophys J. 1996;71(6):3430–3441.Google Scholar
Suh, R, Takayama, S, Smith, GD. Microfluidic applications for andrology. J Androl. 2005;26(6):664–670.Google Scholar
Quinn, MM, Jalalian, L, Ribeiro, S, et al. Microfluidic sorting selects sperm for clinical use with reduced DNA damage compared to density gradient centrifugation with swim-up in split semen samples. Hum Reprod. 2018; 33(8):1388–1393.Google Scholar
De Wagenaar, B, Dekker, S, De Boer, HL, et al. Towards microfluidic sperm refinement: impedance-based analysis and sorting of sperm cells. Lab Chip. 2016;16(8):1514–1522.Google Scholar
Ohta, AT, Garcia, M, Valley, JK, et al. Motile and non-motile sperm diagnostic manipulation using optoelectronic tweezers. Lab Chip. 2010;10(23):3213–3217.Google Scholar
Huang, SB, Wu, MH, Lin, YH, et al. High-purity and label-free isolation of circulating tumor cells (CTCs) in a microfluidic platform by using optically-induced-dielectrophoretic (ODEP) force. Lab Chip. 2013; 13(7):1371–1383.Google Scholar
Shuchat, S, Park, S, Kol, S, Yossifon, G. Distinct and independent dielectrophoretic behavior of the head and tail of sperm and its potential for the safe sorting and isolation of rare spermatozoa. Electrophoresis. 2019;40(11):1606–1614.Google Scholar
Liu, W, Chen, W, Liu, R, et al. Separation of sperm and epithelial cells based on the hydrodynamic effect for forensic analysis. Biomicrofluidics. 2015; 9(4):044127.Google Scholar
Takagi, J, Yamada, M, Yasuda, M, Seki, M. Continuous particle separation in a microchannel having asymmetrically arranged multiple branches. Lab Chip. 2005;9(11):1638–1639.Google Scholar
Berendsen, JTW, Eijkel, JCT, Wetzels, AM, Segerink, LI. Separation of spermatozoa from erythrocytes using their tumbling mechanism in a pinch flow fractionation device. Microsystems Nanoeng. 2019;5:24.Google Scholar
Son, J, Murphy, K, Samuel, R, Gale, BK, Carrell, DT, Hotaling, JM. Non-motile sperm cell separation using a spiral channel. Anal Methods. 2015;7:8041–8047.Google Scholar
Son, J, Samuel, R, Gale, BK, Carrell, DT, Hotaling, JM. Separation of sperm cells from samples containing high concentrations of white blood cells using a spiral channel. Biomicrofluidics. 2017;11(5):054106.Google Scholar
Vermes, I, Haanen, C, Steffens-Nakken, H, Reutellingsperger, C. A novel assay for apoptosis flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods. 1995;184(1):39–51.Google Scholar
Glander, HJ, Schaller, J. Binding of annexin V to plasma membranes of human spermatozoa: a rapid assay for detection of membrane changes after cryostorage. Mol Hum Reprod. 1999;5(2):109–115.Google Scholar
Paasch, U, Grunewald, S, Fitzl, G, Glander, HJ. Deterioration of plasma membrane is associated with activated caspases in human spermatozoa. J Androl. 2003;24(2):246–252.Google Scholar
Gil, M, Sar-Shalom, V, Melendez Sivira, Y, Carreras, R, Checa, MA. Sperm selection using magnetic activated cell sorting (MACS) in assisted reproduction: a systematic review and meta-analysis. J Assist Reprod Genet. 2013;30(4):479–485.Google Scholar
Said, TM, Grunewald, S, Paasch, U, et al. Advantage of combining magnetic cell separation with sperm preparation techniques. Reprod Biomed Online. 2005;10(6):740–746.Google Scholar
Grunewald, S, Reinhardt, M, Blumenauer, V, et al. Increased sperm chromatin decondensation in selected nonapoptotic spermatozoa of patients with male infertility. Fertil Steril. 2009;92(2):572–577.Google Scholar
Dirican, EK, Özgün, OD, Akarsu, S, et al. Clinical outcome of magnetic activated cell sorting of non-apoptotic spermatozoa before density gradient centrifugation for assisted reproduction. J Assist Reprod Genet. 2008;25(8):375–381.Google Scholar
Picot, J, Guerin, CL, Le Van, Kim C, Boulanger, CM. Flow cytometry: retrospective, fundamentals and recent instrumentation. Cytotechnology. 2012;64(2):109–130.Google Scholar
Komoda, T, Matsunaga, T. Biotechnological study. In: Biochemistry for Medical Professionals. Elsevier; 2015:75–93.Google Scholar
Mittal, S, Mielnik, A, Bolyakov, A, Schlegel, P, Paduch, D. PD68–01 pilot study results using fluorescence activated cell sorting of spermatozoa from testis tissue: a novel method for sperm isolation after TESE. J Urol. 2017;197:e139.Google Scholar
Štiavnická, M, Abril-Parreño, L, Nevoral, J, Králícková, M, García-Álvarez, O. Non-invasive approaches to epigenetic-based sperm selection. Med Sci Monit. 2017;23:4677–4683.Google Scholar
Amaral, S, Da Costa, R, Wübbeling, F, Redmann, K, Schlatt, S. Raman micro-spectroscopy analysis of different sperm regions: a species comparison. Mol Hum Reprod. 2018;24(4):185–202.Google Scholar
Ramser, K. Raman spectroscopy of single cells for biomedical applications. In: Ghomi, M, ed. Applications of Raman Spectroscopy to Biology: From Basic Studies to Disease Diagnosis. IOS Press; 2012:106–147.Google Scholar

References

Whitesides, G. The origins and the future of microfluidics. Nature. 2006;442(7101):368–373. doi:10.1038/nature05058Google Scholar
Hu, C, Chen, Y, Tan, MJA, Ren, K, Wu, H. Microfluidic technologies for vasculature biomimicry. Analyst. 2019;144(15):4461–4471. doi:10.1039/c9an00421aGoogle Scholar
Kaushik, G, Leijten, J, Khademhosseini, A. Concise review: organ engineering: design, technology, and integration. Stem Cells. 2017;35(1):55–60. doi:10.1002/stem.2502Google Scholar
Pamme, N. Continuous flow separations in microfluidic devices. Lab Chip. 2007;7:1644–1659. doi:10.1039/b712784gGoogle Scholar
Feng, H, Magda, JJ, Gale, BK. Viscoelastic second normal stress difference dominated multiple-stream particle focusing in microfluidic channels. Appl Phys Lett. 2019;115(26). doi:10.1063/1.5129281Google Scholar
Jin, D, Deng, B, Li, JX, et al. A microfluidic device enabling high-efficiency single cell trapping. Biomicrofluidics. 2015;9(1):014101. doi:10.1063/1.4905428Google Scholar
Schibel, AEP, Ervin, EN. Decreasing the limits of detection and analysis time of ion current rectification biosensing measurements via a mechanically applied pressure differential. Anal Chem. 2015;87(13): 6646–6653. doi:10.1021/acs.analchem.5b00757Google Scholar
Convery, N, Gadegaard, N. 30 years of microfluidics. Micro Nano Eng. 2019;2:76–91. doi:10.1016/j.mne.2019.01.003Google Scholar
Kashaninejad, N, Shiddiky, MJA, Nguyen, N-T, Kashaninejad, N, Nguyen, N-T, Shiddiky, MJA. Advances in microfluidics-based assisted reproductive technology: from sperm sorter to reproductive system-on-a-chip. Adv Biosyst. 2018;2(3):1700197. doi:10.1002/adbi.201700197Google Scholar
Smith, GD, Takayama, S. Application of microfluidic technologies to human assisted reproduction. Mol Hum Reprod. 2017;23(4):257–268. doi:10.1093/molehr/gaw076Google Scholar
Samuel, R, Badamjav, O, Murphy, KE, et al. Microfluidics: the future of microdissection TESE? Syst Biol Reprod Med. 2016;62(3). doi:10.3109/19396368.2016.1159748Google Scholar
Schuster, TG, Cho, B, Keller, LM, Takayama, S, Smith, GD. Isolation of motile spermatozoa from semen samples using microfluidics. Reprod Biomed Online. 2003;7(1):75–81. doi:10.1016/S1472-6483(10)61732-4Google Scholar
Oseguera-López, I, Ruiz-Díaz, S, Ramos-Ibeas, P, Pérez-Cerezales, S. Novel techniques of sperm selection for improving IVF and ICSI outcomes. Front Cell Dev Biol. 2019;7. doi:10.3389/fcell.2019.00298Google Scholar
Chinnasamy, T, Kingsley, JL, Inci, F, et al. Guidance and self-sorting of active swimmers: 3D periodic arrays increase persistence length of human sperm selecting for the fittest. Adv Sci. 2018;5(2):1700531. doi:10.1002/advs.201700531Google Scholar
Quinn, MM, Jalalian, L, Ribeiro, S, et al. Microfluidic sorting selects sperm for clinical use with reduced DNA damage compared to density gradient centrifugation with swim-up in split semen samples. Hum Reprod. 2018;33(8):1388–1393. doi:10.1093/humrep/dey239Google Scholar
Knowlton, SM, Sadasivam, M, Tasoglu, S. Microfluidics for sperm research. Trends Biotechnol. 2015;33(4):221–229. doi:10.1016/j.tibtech.2015.01.005Google Scholar
Zhang, X, Khimji, I, Gurkan, UA, et al. Lensless imaging for simultaneous microfluidic sperm monitoring and sorting. Lab Chip. 2011;11(15):2535–2540. doi:10.1039/c1lc20236gGoogle Scholar
Asghar, W, Velasco, V, Kingsley, JL, et al. Selection of functional human sperm with higher DNA integrity and fewer reactive oxygen species. Adv Healthc Mater. 2014;3(10):1671–1679. doi:10.1002/adhm.201400058Google Scholar
Nosrati, R, Vollmer, M, Eamer, L, et al. Rapid selection of sperm with high DNA integrity. Lab Chip. 2014;14(6):1142–1150. doi:10.1039/c3lc51254aGoogle Scholar
Gaffney, EA, Gadêlha, H, Smith, DJ, Blake, JR, Kirkman-Brown, JC. Mammalian sperm motility: observation and theory. Annu Rev Fluid Mech. 2011;43(1):501–528. doi:10.1146/annurev-fluid-121108-145442Google Scholar
Chen, Y-A, Huang, Z-W, Tsai, F-S, Chen, C-Y, Lin, C-M, Wo, AM. Analysis of sperm concentration and motility in a microfluidic device. Microfluid Nanofluidics. 2011;10(1):59–67. doi:10.1007/s10404-010-0646-8Google Scholar
Xie, L, Ma, R, Han, C, et al. Integration of sperm motility and chemotaxis screening with a microchannel-based device. Clin Chem. 2010;56(8):1270–1278. doi:10.1373/clinchem.2010.146902Google Scholar
Ma, R, Xie, L, Han, C, et al. In vitro fertilization on a single-oocyte positioning system integrated with motile sperm selection and early embryo development. Anal Chem. 2011;83(8):2964–2970. doi:10.1021/ac103063gGoogle Scholar
Li, Z, Liu, W, Qiu, T, et al. The construction of an interfacial valve-based microfluidic chip for thermotaxis evaluation of human sperm. Biomicrofluidics. 2014;8(2):024102. doi:10.1063/1.4866851Google Scholar
Liu, W, Chen, W, Liu, R, et al. Separation of sperm and epithelial cells based on the hydrodynamic effect for forensic analysis. Biomicrofluidics. 2015;9(4):044127. doi:10.1063/1.4928453Google Scholar
Son, J, Murphy, K, Samuel, R, Gale, BK, Carrell, DT, Hotaling, JM. Non-motile sperm cell separation using a spiral channel. Anal Methods. 2015;7:1–7. doi:10.1039/C5AY02205CGoogle Scholar
Son, J, Samuel, R, Gale, BK, Carrell, DT, Hotaling, JM. Separation of sperm cells from samples containing high concentrations of white blood cells using a spiral channel. Biomicrofluidics. 2017;11(5):054106. doi:10.1063/1.4994548Google Scholar
Rosales-Cruzaley, E, Cota-Elizondo, PA, Sánchez, D, Lapizco-Encinas, BH. Sperm cells manipulation employing dielectrophoresis. Bioprocess Biosyst Eng. 2013;36(10):1353–1362. doi:10.1007/s00449-012-0838-6Google Scholar
de Wagenaar, B, Dekker, S, de Boer, HL, et al. Towards microfluidic sperm refinement: impedance-based analysis and sorting of sperm cells. Lab Chip. 2016;16(8):1514–1522. doi:10.1039/C6LC00256KGoogle Scholar
Cho, BS, Schuster, TG, Zhu, X, Chang, D, Smith, GD, Takayama, S. Passively driven integrated microfluidic system for separation of motile sperm. Anal Chem. 2003;75(7):1671–1675. doi:10.1021/ac020579eGoogle Scholar
Shirota, K, Yotsumoto, F, Itoh, H, et al. Separation efficiency of a microfluidic sperm sorter to minimize sperm DNA damage. Fertil Steril. 2016;105(2):315–321. doi:10.1016/j.fertnstert.2015.10.023Google Scholar
Wu, J-K, Chen, P-C, Lin, Y-N, Wang, C-W, Pan, L-C, Tseng, F-G. High-throughput flowing upstream sperm sorting in a retarding flow field for human semen analysis. Analyst. 2017;142(6):938–944. doi:10.1039/C6AN02420CGoogle Scholar
Horsman, KM, Barker, SLR, Ferrance, JP, Forrest, KA, Koen, KA, Landers, JP. Separation of sperm and epithelial cells in a microfabricated device: potential application to forensic analysis of sexual assault evidence. Anal Chem. 2005;77(3):742–749. doi:10.1021/ac0486239Google Scholar
Phiphattanaphiphop, C, Leksakul, K, Phatthanakun, R, Suthummapiwat, A. Real-time single cell monitoring: measurement and counting of motile sperm using LCR impedance-integrated microfluidic device. Micromachines. 2019;10(10):647. doi:10.3390/mi10100647Google Scholar
Segerink, LI, Sprenkels, AJ, ter Braak, PM, Vermes, I, van den Berg, A. On-chip determination of spermatozoa concentration using electrical impedance measurements. Lab Chip. 2010;10(8):1018–1024. doi:10.1039/b923970gGoogle Scholar
Samuel, R, Feng, H, Jafek, A, Despain, D, Jenkins, T, Gale, B. Microfluidic-based sperm sorting & analysis for treatment of male infertility. Transl Androl Urol. 2018;7(S3):S336–S347. doi:10.21037/tau.2018.05.08Google Scholar
Gode, F, Bodur, T, Gunturkun, F, et al. Comparison of microfluid sperm sorting chip and density gradient methods for use in intrauterine insemination cycles. Fertil Steril. 2019;112(5):842–848.e1. doi:10.1016/j.fertnstert.2019.06.037Google Scholar
Jafek, A, Feng, H, Brady, H, et al. An automated instrument for intrauterine insemination sperm preparation. Sci Rep. 2020;10(1):21385. doi:10.1038/s41598-020-78390-3Google Scholar
Jenkins, T, Samuel, R, Jafek, A, et al. Rapid microfluidic sperm isolation from microtese samples in men with non-obstructive azoospermia. Fertil Steril. 2017;108(3):e244. doi:10.1016/j.fertnstert.2017.07.733Google Scholar

References

Shehata, F, Chian, RC. Cryopreservation of sperm: an overview. In: Chian, RC, Quinn, P, eds. Fertility Cryopreservation. Cambridge University Press; 2010:39–45.Google Scholar
Sherman, JK. Synopsis of the use of frozen human semen since 1964: state of the art of human semen banking. Fertil Steril. 1973;24:397–412.Google Scholar
Bunge, RG, Sherman, JK. Fertilizing capacity of frozen human spermatozoa. Nature. 1953;172:767–768.Google Scholar
Li, K, Rodriguez, D, Gabrielsen, JS, Centola, GM, Tanrikut, C. Transgender sperm cryopreservation: trends and findings in the past decade. Andrology. 2018;6(6):860–864.Google Scholar
Alouf, CA, Celia, G, Centola, GM. Sperm cryopreservation – a practical guide. In: Allahbadia, GN, Ata, B, Lindheim, SR, Woodward, BJ, Bhagavath, B, eds. Textbook of Assisted Reproduction. Springer; 2019:497–504.Google Scholar
Centola, GM, Sperm banking, donation, and transport in the age of assisted reproduction: federal and state regulation. In: Carrell, DT, Peterson, CM, eds. Reproductive Endocrinology and Infertility: Integrating Modern Clinical and Laboratory Practice. Springer; 2010:509–516.Google Scholar
Di Santo, M, Tarozzi, N, Nadalini, M, Borini, A. Human sperm cryopreservation: update on techniques, effect on DNA integrity, and implications for ART. Adv Urol. 2012;2012:854837.Google Scholar
Kong, A, Frigge, ML, Masson, G, et al. Rate of de novo mutations and the importance of father’s age to disease risk. Nature. 2012;488(7412):471–475.Google Scholar
Centola, GM, Blanchard, A, Demick, J, Li, S, Eisenberg, M. Decline in sperm count and motility in young adult men from 2003–2013: observations from a U.S. sperm bank. Andrology. 2016;4(3):270–276.Google Scholar
Sharma, R, Agarwal, A, Rohra, VK, Assidi, M, Abu-Elmagd, M, Turki, RF. Effects of increased paternal age on sperm quality, reproductive outcome and associated genetic risks to offspring. Reprod Biol Endoc. 2015;13:35.Google Scholar
D’Onofrio, BM, Rickert, ME, Frans, E, et al. Paternal age at childbearing and offspring psychiatric and academic morbidity. JAMA Psychiatry. 2014;71(4):432–438.Google Scholar
Pacey, AA. Referring patients for sperm banking. In: Pacey, AA, Tomlinson, MJ, eds. Sperm Banking: Theory and Practice. Cambridge University Press; 2009:30–40.Google Scholar
New York State, Part 52, Tissue Banks and Non Transplant Anatomic Banks, Public Health Section 4365; Subpart 52–58; www.wadsworth.org/regulatory/btrp/laws. Accessed November 9, 2022.Google Scholar
US Food and Drug Administration, 21 CFR 1271; www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=1271. Accessed November 9, 2022.Google Scholar
California Department of Public Health (CDPH) Tissue Bank Regulation, Article 2. 1639–1641.1. https://leginfo.legislature.ca.gov/faces/codes_displayText.xhtml?lawCode=HSC&division=2.&title=&part=&chapter=4.1.&article=2. Accessed November 9, 2022.Google Scholar
Practice Committee of American Society for Reproductive Medicine and the Practice Committee of Society for Assisted Reproductive Technology. Recommendations for gamete and embryo donation: a committee opinion. Fertil Steril. 2013;99(1):47–62.Google Scholar
American Association of Tissue Bank. Standards for Tissue Banking, 14th ed., January 31, 2020. https://static1.squarespace.com/static/5f2dc76b6a743f2147b29a37/t/5f3334d90f2540201689051c/1597191396553/AATB+Standards+for+Tissue+Banking+-14th+Edition-+-+-Posted+8-3-16-.pdf. Accessed November 9, 2022.Google Scholar
Shuster, TG, Hickner-Cruz, K, Ohl, DA, Goldman, E, Smith, G. Legal considerations for cryopreservation of sperm and embryos. Fertil Steril. 2003;80:61–66.Google Scholar
Joint Commission. Informed consent: more than getting a signature. www.jointcommission.org/-/media/tjc/documents/newsletters/quick_safety_issue_twenty-one_february_2016pdf.pdfGoogle Scholar
Centola, GM. Sperm or no sperm, that is the question! Finding the elusive spermatozoa. Fertil Steril. 2012;98:822.Google Scholar
Centola, GM, Raubertas, RF, Mattox, JH. Cryopreservation of human semen: comparison of cryopreservatives, sources of variability and prediction of post-thaw survival. J Androl. 1992;13(3):283–288.Google Scholar
Cohen, J, Garrisi, GJ, Congedo-Ferrara, TA, Kieck, KA, Sehimmel, TW, Scott, RT. Cryopreservation of single human spermatozoa. Hum Reprod. 1997;12:994–1001.Google Scholar
Gvakharia, M, Adamson, G. A method of successful cryopreservation of small numbers of human spermatozoa. Fertil Steril. 2001;76:S101.Google Scholar
Desai, NN, Culler, C, Goldfarb, J. Cryopreservation of single sperm from epidermal and testicular samples on cryoloops: preliminary case report. Fertil Steril. 2004;82:S264.Google Scholar
Isachemko, V, Isachenko, E, Montag, M, et al. Clean technique for cryoprotectant-free vitrification of human spermatozoa. RBMO. 2005;10:350–354.Google Scholar
Centola, GM, Allen, J. The ability of sperm to survive cryopreservation is not related to initial sperm concentration. Paper presented at the American Society of Andrology Annual Meeting, April 1993.Google Scholar
Nagy, Z, Liu, J, Cecile, J, Silber, S, Devroey, P, Van Steirteghem, A. Using ejaculated, fresh, and frozen-thawed epididymal and testicular spermatozoa gives rise to comparable results after intracytoplasmic sperm injection. Fertil Steril. 1995;63(4):808–815.Google Scholar
Yu, Z, Wei, Z, Yang, J, et al. Comparison of intracytoplasmic sperm injection outcome with fresh versus frozen-thawed testicular sperm in men with nonobstructive azoospermia: a systematic review and meta-analysis. J Assist Reprod Genet. 2018;35(7):1247–1257.Google Scholar
Kuczyński, W, Dhont, M, Grygoruk, C, Grochowski, D, Wołczyński, S, Szamatowicz, M. The outcome of intracytoplasmic injection of fresh and cryopreserved ejaculated spermatozoa: a prospective randomized study. Hum Reprod. 2001;16(10):2109–2113.Google Scholar
Ragni, G, Caccamo, AM, Dalla Serra, A, Guercilena, S. Computerized slow-staged freezing of semen from men with testicular tumors or Hodgkin’s disease preserves sperm better than standard vapor freezing. Fertil Steril. 1990;53(6):1072–1075.Google Scholar
Ragni, G, Somigliana, E, Restelli, L, Salvi, R, Arnoldi, M, Paffoni, A. Sperm banking and rate of assisted reproduction treatment: insights from a 15 year cryopreservation program for male cancer patients. Cancer. 2003;97(7):1624–1629.Google Scholar
Borges, E, Jr., Rossi, LM, Locambo de Freitas, CV, et al. Fertilization and pregnancy outcome after intracytoplasmic injection with fresh or cryopreserved ejaculated spermatozoa. Fertil Steril. 2007;87(2):316–320.Google Scholar
Gerkowicz, SA, Crawford, S, Hipp, H, Boulet, S, Kissin, DM, Kawwass, JF. Assisted reproductive technology with donor sperm: national trends and perinatal outcomes. Fertil Steril. 2017;108(3):e72.Google Scholar
Fritz, R, Jindal, S, Yu, B, Vega, M, Buyuk, E. Does donor sperm affect birth weight, preterm birth, and miscarriage rates in fresh autologous in vitro fertilization cycles? Analysis of 46.061 cycles reported to SART. Fertil Steril. 2017;107(3):e30.Google Scholar
Malchau, SS, Loft, A, Henningsen, A-K, Andersen, AN, Pinborg, A. Perinatal outcomes in 6338 singletons born after intrauterine insemination in Denmark, 2007 to 2012: the influence of ovarian stimulation. Fertil Steril. 2014;102:1110–1116.Google Scholar
Shin, DH, Turek, PJ. Sperm retrieval techniques. Nature Rev Urology. 2013;10:723–730.Google Scholar
Devroey, P, Silber, S, Nagy, Z, et al. Ongoing pregnancies and births after intracytoplasmic sperm injection with frozen-thawed epididymal spermatozoa. Hum Reprod. 1995;10:903–906.Google Scholar
Fischer, R, Baukloh, V, Naether, OGJ, Schulze, W, Salzbrunn, A, Benson, DM. Pregnancy after intracytoplasmic sperm injection of spermatozoa extracted from frozen-thawed testicular biopsy. Hum Reprod. 1996;11:2197–2199.Google Scholar
Gil-Slamon, M, Romeo, J, Mingues, Y. Pregnancies after intracytoplasmic sperm injection with cryopreserved testicular sperm. Hum Reprod. 1996;11:1309–1313.Google Scholar
Patrizio, P, Natan, Y, Barak, Y, Levi Setti, P. A simple new method for the freeze-drying and storage of human sperm. Fertil Steril. 2016;106(3):e307.Google Scholar
Frydman, R, Grynberg, M. Male fertility preservation: innovations and questions. Fertil Steril. 2015;105:247–248.Google Scholar
Moss, JL, Choi, A, Keeter, MKF, Brannigan, RE. Male adolescent fertility preservation. Fertil Steril. 2015;105(2):267–273.Google Scholar
Gies, I, Oates, R, De Schepper, J, Tournaye, H. Testicular biopsy and cryopreservation for fertility preservation of prepubertal boys with Klinefelter syndrome: a pro/con debate. Fertil Steril. 2016;105(2):249–255.Google Scholar
Gassei, K, Orwig, KE. Experimental methods to preserve male fertility and treat male factor infertility. Fertil Steril. 2016;105(2):256–266.Google Scholar
Sinha, N, Whelan, EC, Brinster, RL. Isolation, cryopreservation, and transplantation of spermatogonial stem cells. Methods Mol Biol. 2019;2005:205–220.Google Scholar
Valli, H, Phillips, BT, Shetty, G, et al. Germline stem cells: toward the regeneration of spermatogenesis. Fertil Steril. 2014;101(1):3–13.Google Scholar
Goossens, E, Van Saen, D, Tournaye, H. Spermatogonial stem cell preservation and transplantation: from research to clinic. Hum Reprod. 2013;28:897–907.Google Scholar
Fertility preservation program of Magee-Womens Hospital in Pittsburgh. https://mageewomens.org/for-researchers/research-centers/fertility-preservation-program-fpp#:~:text=The%20Fertility%20Preservation%20Program%20in%20Pittsburgh%20is%20committed%20to%3A,preserve%20fertility%20and%20treat%20infertility.Google Scholar

References

Anawalt, BD. Approach to male infertility and induction of spermatogenesis. J Clin Endocrinol Metab. 2013;98(9):3532–3542.Google Scholar
Levine, H, Jorgensen, N, Martino-Andrade, A, et al. Temporal trends in sperm count: a systematic review and meta regression analysis. Hum Reprod Update. 2017;23:646–659.Google Scholar
Sharpe, RM, Franks, S. Environment, lifestyle, and infertility: an inter-generational issue. Nat Cell Biol. 2002;s33–s40.Google Scholar
Van Batavia, JP, Kolon, TF. Fertility in disorders of sex development. J Pediatr Urol. 2016;12(6):418–425.Google Scholar
Gomes, NL, Chetty, T, Jorgensen, A, Mitchell, RT. Disorders of sex development: novel regulators, impacts on fertility, and options for fertility preservation. Int J Mol Sci. 2020;21(7):2282.Google Scholar
Picton, HM, Wyns, C, Anderson, RA, et al. ESHRE task force on fertility preservation in severe diseases: a European perspective on testicular tissue cryopreservation for fertility preservation in prepubertal and adolescent boys. Hum Reprod. 2015;30(11):2463–2475.Google Scholar
Weblink: www.urologyhealth.org/urologic-conditions/male-infertilityGoogle Scholar
Gassei, K, Orwig, KE. Experimental methods to preserve male fertility and treat male infertility. Fertil Steril. 2016;105(2):256–266.Google Scholar
Horwich, A, Shipley, J, Huddart, R. Testicular germ-cell cancer. Lancet. 2006;367:754–765.Google Scholar
Rajpert-De Meyts, E, McGlynn, KA, Okamoto, K, Jewett, MAS, Bokemeyer, C. Testicular germ cell tumours. Lancet. 2016;387:1762–1774.Google Scholar
Sharma, S, Wistuba, J, Pock, T, Schlatt, S, Neuhaus, N. Spermatogonial stem cells: updates from specification to clinical relevance. Hum Reprod Update. 2019;25(3):275–297.Google Scholar
Goossens, E, Jahnukainen, K, Mitchell, RT, et al. Fertility preservation in boys: recent developments and new insights. Hum Reprod Open. 2020;2020(3):hoaa016.Google Scholar
Oncofertility Consortium. Homepage. https://oncofertility.northwestern.edu/Google Scholar
Schlatt, S, Ehmcke, J. Regulation of spermatogenesis: an evolutionary biologist’s perspective. Semin Cell Dev Biol. 2014;29:2–16.Google Scholar
Tung, PS, Fritz, IB. Interactions of Sertoli cells with myoid cells in vitro. Biol Reprod. 1980;23:207–217.Google Scholar
Hadley, MA, Byers, SW, Suárez-Quian, CA, Kleinman, HK, Dym, M. Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation, and germ cell development in vitro. J Cell Biol. 1985;101:1511–1522.Google Scholar
Kierszenbaum, AL, Crowell, JA, Shabanowitz, RB, DePhilip, RM, Tres, LL. Protein secretory patterns of rat Sertoli and peritubular cells are influenced by culture conditions. Biol Reprod. 1986;35:239–251.Google Scholar
Tung, PS, Fritz, IB. Extracellular matrix components and testicular peritubular cells influence the rate and pattern of Sertoli cell migration in vitro. Dev Biol. 1986; 113:119–134.Google Scholar
Tung, PS, Fritz, IB. Morphogenetic restructuring and formation of basement membranes by Sertoli cells and testis peritubular cells in co-culture: inhibition of the morphogenetic cascade by cyclic AMP derivatives and by blocking direct cell contact. Dev Biol. 1987;120:139–153.Google Scholar
Hofmann, MC, Narisawa, S, Hess, RA, Millan, JL. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp Cell Res. 1992;201:417–435.Google Scholar
Richardson, LL, Kleinman, HK, Dym, M. Basement membrane gene expression by Sertoli and peritubular myoid cells in vitro in the rat. Biol Reprod. 1995;52:320–330.Google Scholar
Schlatt, S, de Kretser, DM, Loveland, KL. Discriminative analysis of rat Sertoli and peritubular cells and their proliferation in vitro: evidence for follicle-stimulating hormonemediated contact inhibition of Sertoli cell mitosis. Biol Reprod. 1996;55:227–235.Google Scholar
van der Wee, K, Hofmann, MC. An in vitro tubule assay identifies HGF as a morphogen for the formation of seminiferous tubules in the postnatal mouse testis. Exp Cell Res. 1999;252:175–185.Google Scholar
Hoeben, E, Swinnen, JV, Heyns, W, Verhoeven, G. Heregulins or neu differentiation factors and the interactions between peritubular myoid cells and Sertoli cells. Endocrinology. 1999;140:2216–2223.Google Scholar
El Ramy, R, Verot, A, Mazaud, S, Odet, F, Magre, S, Le Magueresse-Battistoni, B. Fibroblast growth factor (FGF) 2 and FGF9 mediate mesenchymal–epithelial interactions of peritubular and Sertoli cells in the rat testis. J Endocrinol. 2005;187:135–147.Google Scholar
Gassei, K, Schlatt, S, Ehmcke, J. De novo morphogenesis of seminiferous tubules from dissociated immature rat testicular cells in xenografts. J Androl. 2006;27:611–618.Google Scholar
Marcon, L, Zhang, X, Hales, BF, Nagano, MC, Robaire, B. Development of a short term fluorescence-based assay to assess the toxicity of anticancer drugs on rat stem/progenitor spermatogonia in vitro. Biol Reprod. 2010;83:228–237.Google Scholar
Mincheva, M, Sandhowe-Klaverkamp, R, Wistuba, J, et al. Reassembly of adult human testicular cells: can testis cord-like structures be created in vitro? Mol Hum Reprod. 2018;24(2):55–63.Google Scholar
von Kopylow, K, Schulze, W, Salzbrunn, A, et al. Mol Hum Reprod. 2018; 24(3):123–134.Google Scholar
Mincheva, M, Wistuba, J, Brenker, C, Schlatt, S. Challenging human somatic testicular cell reassembly by protein kinase inhibtion: setting up a functional in vitro test system. Sci Rep. 2020;10(1):8935.Google Scholar
Iwanami, Y, Kobayashi, T, Kato, M, Hirabayashi, M, Hochi, S. Characteristics of rat round spermatids differentiated from spermatogonial cells during co-culture with Sertoli cells, assessed by flow cytometry, microinsemination and RT-PCR. Theriogenology. 2006;65:288–298.Google Scholar
Xie, B, Qin, Z, Huang, B, et al. In vitro culture and differentiation of buffalo (Bubalus bubalis) spermatogonia. Reprod Domest Anim. 2010;45:275–282Google Scholar
Tres, LL, Kierszenbaum, AL. Viability of rat spermatogenic cells in vitro is facilitated by their coculture with Sertoli cells in serum-free hormone-supplemented medium. Proc Natl Acad Sci USA. 1983;80:3377–3381.Google Scholar
Tesarik, J, Greco, E, Rienzi, L, et al. Differentiation of spermatogenic cells during in-vitro culture of testicular biopsy samples from patients with obstructive azoospermia: effect of recombinant follicle stimulating hormone. Hum Reprod. 1998a;13:2772–2781.Google Scholar
Tesarik, J, Guido, M, Mendoza, C, Greco, E. Human spermatogenesis in vitro: respective effects of follicle-stimulating hormone and testosterone on meiosis, spermiogenesis, and Sertoli cell apoptosis. J Clin Endocrinol Metab. 1998b;83:4467–4473.Google Scholar
Tesarik, J, Balaban, B, Isiklar, A, et al. In-vitro spermatogenesis resumption in men with maturation arrest: relationship with in-vivo blocking stage and serum FSH. Hum Reprod. 2000;15:1350–1354.Google Scholar
Sousa, M, Cremades, N, Alves, C, Silva, J, Barros, A. Developmental potential of human spermatogenic cells co-cultured with Sertoli cells. Hum Reprod. 2002;17:161–172.Google Scholar
Tanaka, A, Nagayoshi, M, Awata, S, Mawatari, Y, Tanaka, I, Kusunoki, H. Completion of meiosis in human primary spermatocytes through in vitro coculture with Vero cells. Fertil Steril. 2003;79:795–801.Google Scholar
Vigier, M, Weiss, M, Perrard, MH, Godet, M, Durand, P. The effects of FSH and of testosterone on the completion of meiosis and the very early steps of spermiogenesis of the rat: an in vitro study. J Mol Endocrinol. 2004;33:729–742.Google Scholar
Nagao, Y. Viability of meiotic prophase spermatocytes of rats is facilitated in primary culture of dispersed testicular cells on collagen gel by supplementing epinephrine or norepinephrine: evidence that meiotic prophase spermatocytes complete meiotic divisions in vitro. In Vitro Cell Dev Biol. 1989;25:1088–1098.Google Scholar
Magueresse-Battistoni, BL, Gérard, N, Jégou, B. Pachytene spermatocytes can achieve meiotic process in vitro. Biochem Biophys Res Commun. 1991;179(2):1115–1121.Google Scholar
Cremades, N, Bernabeu, R, Barros, A, Sousa, M. In-vitro maturation of round spermatids using co-culture on Vero cells. Hum Reprod. 1999;14:1287–1293.Google Scholar
Enders, GC, Henson, JH, Millette, CF. Sertoli cell binding to isolated testicular basement membrane. J Cell Biol. 1986;103:1109–1119.Google Scholar
Hadley, MA, Weeks, BS, Kleinman, HK, Dym, M. Laminin promotes formation of cord-like structures by Sertoli cells in vitro. Dev Biol. 1990;140:318–327.Google Scholar
Gassei, K, Ehmcke, J, Schlatt, S. Initiation of testicular tubulogenesis is controlled by neurotrophic tyrosine receptor kinases in a three-dimensional Sertoli cell aggregation assay. Reproduction. 2008;136:459–469.Google Scholar
Yu, X, Hong, S, Moreira, EG, Faustman, EM. Improving in vitro Sertoli cell/gonocyte co-culture model for assessing male reproductive toxicity: lessons learned from comparisons of cytotoxicity versus genomic responses to phthalates. Toxicol Appl Pharmacol. 2009;239:325–336.Google Scholar
Gassei, K, Ehmcke, J, Wood, MA, Walker, WH, Schlatt, S. Immature rat seminiferous tubules reconstructed in vitro express markers of Sertoli cell maturation after xenografting into nude mouse hosts. Mol Hum Reprod. 2010;16:97–110.Google Scholar
Pan, F, Chi, LF, Schlatt, S. Effects of nanostructures and mouse embryonic stem cells on in vitro morphogenesis of rat testicular cords. PLoS ONE. 2013;8:e60054.Google Scholar
Wegner, S, Hong, S, Yu, X, Faustman, EM. Preparation of rodent testis co-cultures. Curr Protoc Toxicol. 2013;Chapter 16:Unit 16.10.Google Scholar
Reuter, K, Ehmcke, J, Stukenborg, JB, et al. Reassembly of somatic cells and testicular organogenesis in vitro. Tissue Cell. 2014;46:86–96.Google Scholar
Potter, SJ, DeFalco, T. Using ex vivo upright droplet cultures of whole fetal organs to study developmental processes during mouse organogenesis. J Vis Exp. 2015;e53262.Google Scholar
Harris, S, Hermsen, SAB, Yu, XZ, Hong, SW, Faustman, EM. Comparison of toxicogenomic responses to phthalate ester exposure in an organotypic testis co-culture model and responses observed in vivo. Reprod Toxicol. 2015;58:149–159.Google Scholar
Harris, S, Shubin, SP, Wegner, S, et al. The presence of macrophages and inflammatory responses in an in vitro testicular co-culture model of male reproductive development enhance relevance to in vivo conditions. Toxicol In Vitro. 2016;36:210–215.Google Scholar
Sakib, S, Uchida, A, Valenzuela-Leon, P, et al. Formation of organotypic testicular organoids in microwell culture. Biol Reprod. 2019;100(6):1648–1660.Google Scholar
Edmonds, ME, Woodruff, TK. Testicular organoid formation is a property of immature somatic cells, which self-assemble and exhibit long-term hormone-responsive endocrine function. Biofabrication. 2020;12(4):045002.Google Scholar
Baert, Y, Ruetschle, I, Cools, W, et al. A multi-organ chip co-culture of liver and testis equivalents: a first step toward a systemic male reprotoxicity model. Hum Reprod. 2020;35(5):1029–1044.Google Scholar
Zenzes, MT, Engel, W. The capacity of testicular cells of the postnatal rat to reorganize into histotypic structures. Differentiation. 1981;20:157–161.Google Scholar
Lee, DR, Kaproth, MT, Parks, JE. In vitro production of haploid germ cells from fresh or frozen-thawed testicular cells of neonatal bulls. Biol Reprod. 2001;65:873–878.Google Scholar
Lee, DR, Kim, K-S, Yang, YH, et al. Isolation of male germ stem cell-like cells from testicular tissue of non-obstructive azoospermic patients and differentiation into haploid male germ cells in vitro. Hum Reprod. 2006a;21:471–476.Google Scholar
Lee, JH, Kim, HJ, Kim, H, Lee, SJ, Gye, MC. In vitro spermatogenesis by threedimensional culture of rat testicular cells in collagen gel matrix. Biomaterials. 2006b;27:2845–2853.Google Scholar
Legendre, A, Froment, P, Desmots, S, Lecomte, A, Habert, R, Lemazurier, E. An engineered 3D blood-testis barrier model for the assessment of reproductive toxicity potential. Biomaterials. 2010;31:4492–4505.Google Scholar
Yokonishi, T, Sato, T, Katagiri, K, Komeya, M, Kubota, Y, Ogawa, T. In vitro reconstruction of mouse seminiferous tubules supporting germ cell differentiation. Biol Reprod. 2013;89:11–16.Google Scholar
Zhang, J, Hatakeyama, J, Eto, K, Abe, S. Reconstruction of a seminiferous tubule-like structure in a 3 dimensional culture system of re-aggregated mouse neonatal testicular cells within a collagen matrix. Gen Comp Endocrinol. 2014;205:121–132.Google Scholar
Reda, A, Hou, M, Landreh, L, et al. In vitro spermatogenesis: optimal culture conditions for testicular cell survival, germ cell differentiation, and steroidogenesis in rats. Front Endocrinol (Lausanne). 2014;5:21.Google Scholar
Huleihel, M, Nourashrafeddin, S, Plant, TM. Application of three-dimensional culture systems to study mammalian spermatogenesis, with an emphasis on the rhesus monkey (Macaca mulatta). Asian J Androl. 2015;17:972–980.Google Scholar
Baert, Y, De Kock, J, Alves-Lopes, JP, Söder, O, Stukenborg, J-B, Goossens, E. Primary human testicular cells self-organize into organoids with testicular properties. Stem Cell Reports. 2017;1:30–38.Google Scholar
Baert, Y, Goossens, E. Preparation of scaffolds from decellularized testicular matrix. Methods Mol Biol. 2018;1577:121–127.Google Scholar
Baert, Y, Rombaut, C, Goossens, E. Scaffold-based and scaffold-free testicular organoids from primary human testicular cells. Methods Mol Biol. 2019;1576:283–290.Google Scholar
Baert, Y, Stukenborg, JB, Landreh, M, et al. Derivation and characterization of a cytocompatible scaffold from human testis. Hum Reprod. 2015;30:256–267.Google Scholar
Alves-Lopes, JP, Soder, O, Stukenborg, JB. Testicular organoid generation by a novel in vitro three-layer gradient system. Biomaterials. 2017;130:76–89.Google Scholar
Lee, J-H, Gye, MC, Choi, KW, et al. In vitro differentiation of germ cells from nonobstructive azoospermic patients using three-dimensional culture in a collagen gel matrix. Fertil Steril. 2007;87:824–833.Google Scholar
Lee, JH, Oh, JH, Lee, JH, Kim, MR, Min, CK. Evaluation of in vitro spermatogenesis using poly(D,L-lactic-co-glycolic acid) (PLGA)-based macroporous biodegradable scaffolds. J Tissue Eng Regen Med. 2011;5:130–137.Google Scholar
Zhang, X, Wang, L, Zhang, X, et al. The use of KnockOut serum replacement (KSR) in three dimensional rat testicular cells coculture model: an improved male reproductive toxicity testing system. Food Chem Toxicol. 2017;106:487–495.Google Scholar
Stukenborg, JB, Wistuba, J, Luetjens, CM, et al. Coculture of spermatogonia with somatic cells in a novel three-dimensional soft-agar-culture-system. J Androl. 2008;29:312–329.Google Scholar
Stukenborg, J-B, Schlatt, S, Simoni, M, et al. New horizons for in vitro spermatogenesis? An update on novel three-dimensional culture systems as tools for meiotic and post-meiotic differentiation of testicular germ cells. Mol Hum Reprod. 2009;15:521–529.Google Scholar
Pendergraft, SS, Sadri-Ardekani, H, Atala, A, Bishop, CE. Three-dimensional testicular organoid: a novel tool for the study of human spermatogenesis and gonadotoxicity in vitro dagger. Biol Reprod. 2017;96:720–732.Google Scholar
Elhija, MA, Lunenfeld, E, Schlatt, S, Huleihel, M. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian J Androl. 2012;14:285–293.Google Scholar
Alves-Lopes, JP, Stukenborg, JB. Testicular organoids: a new model to study the testicular microenvironment in vitro? Hum Reprod Update. 2018;24(2):176–191.Google Scholar
Sharma, S, Venzac, B, Burgers, T, Le Gac, S, Schlatt, S. Microfluidics in male reproduction: is ex vivo culture of primate testis tissue a future strategy for ART or toxicology research? Mol Hum Reprod. 2020;26(3):179–192.Google Scholar
Sakib, S, Goldsmith, T, Voigt, A, Dobrinski, I. Testicular organoids to study cell-cell interactions in the mammalian testis. Andrology. 2019; 8(4):835–841.Google Scholar
Komeya, M, Sato, T, Ogawa, T. In vitro spermatogenesis: a century-long research journey, still half way around. Reprod Med Biol. 2018;17(4):407–420.Google Scholar
Gargus, ES, Rogers, HB, McKinnon, KE, Edmonds, ME, Woodruff, TK. Engineered reproductive tissues. Nat Biomed Eng. 2020;4(4):381–393.Google Scholar
Szczepny, A, Hogarth, CA, Young, J, Loveland, KL. Identification of Hedgehog signaling outcomes in mouse testis development using a hanging drop‐culture system. Biol Reprod. 1999;80:258–263.Google Scholar
Jørgensen, A, Young, J, Nielsen, JE, et al. Hanging drop cultures of human testis and testis cancer samples: a model used to investigate activin treatment effects in a preserved niche. Br J Cancer. 2014;110:2604–2614.Google Scholar
Jørgensen, A, Nielsen, JE, Perlman, S, et al. Ex vivo culture of human fetal gonads: manipulation of meiosis signalling by retinoic acid treatment disrupts testis development. Hum Reprod. 2015;30:2351–2363.Google Scholar
Champy, CH. De la méthode de culture des tissus. VI. Le testicule. Arch Zool Exptl Gen. 1920;60:461–500.Google Scholar
Martinovitch, PN. The development in vitro of the mammalian gonad. Ovary and ovogenesis. Proc R Soc B Biol Sci. 1938;125:232–249.Google Scholar
Trowell, OA. The culture of mature organs in a synthetic medium. Exp Cell Res. 1959;16:118–147.Google Scholar
Steinberger, E, Steinberger, A, Perloff, WH. Studies on growth in organ culture of testicular tissue from rats of various ages. Anat Rec. 1964a;148:581–589.Google Scholar
Steinberger, E, Steinberger, A, Perloff, WH. Initiation of spermatogenesis in vitro. Endocrinology. 1964b;74:788–792.Google Scholar
Steinberger, A, Steinberger, E, Perloff, WH. Mammalian testis in organ culture. Exp Cell Res. 1964c;36:19–27.Google Scholar
Steinberger, A, Steinberger, E. Differentiation of rat seminiferous epithelium in organ culture. J Reprod Fertil. 1965;9:243–248.Google Scholar
Steinberger, A, Steinberger, E. Factors affecting spermatogenesis in organ cultures of mammalian testes. J Reprod Fertil. 1967;Suppl. 2:117–124.Google Scholar
Matte, R, Sasaki, M. Autoradiographic evidence of human male germ‐cell differentiation in vitro. Cytologia. 1971;36:298–303.Google Scholar
Boitani, C, Politi, MG, Menna, T. Spermatogonial cell proliferation in organ culture of immature rat testis. Biol Reprod. 1993;48:761–767.Google Scholar
Schlatt, S, Zhengwei, Y, Meehan, T, de Kretser, DM, Loveland, KL. Application of morphometric techniques to postnatal rat testes in organ culture: insights into testis growth. Cell Tissue Res. 1999;298:335–343.Google Scholar
Meehan, T, Schlatt, S, O’Bryan, M, de Kretser, DM, Loveland, KL. Regulation of germ cell and Sertoli cells development by activin, follistatin and FSH. Dev Biol. 2000;220:225–237.Google Scholar
Suzuki, S, Sato, K. The fertilising ability of spermatogenic cells derived from cultured mouse immature testicular tissue. Zygote. 2003;11:307–316.Google Scholar
Lambrot, R, Coffigny, H, Pairault, C, et al. Use of organ culture to study the human fetal testis development: effect of retinoic acid. J Clin Endocrinol Metab. 2006;91:2696–2703.Google Scholar
Roulet, V, Denis, H, Staub, C, et al. Human testis in organotypic culture: application for basic or clinical research. Hum Reprod. 2006;21:1564–1575.Google Scholar
Gohbara, A, Katagiri, K, Sato, T, et al. In vitro murine spermatogenesis in an organ culture system. Biol Reprod. 2010;83:261–267.Google Scholar
Sato, T, Katagiri, K, Gohbara, A, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011a;471:504–507.Google Scholar
Sato, T, Katagiri, K, Yokonishi, T, et al. In vitro production of fertile sperm from murine spermatogonial stem cell lines. Nat Commun. 2011b;2:472.Google Scholar
Dumont, L, Oblette, A, Rondanino, C, et al. Vitamin A prevents round spermatid nuclear damage and promotes the production of motile sperm during in vitro maturation of vitrified prepubertal mouse testicular tissue. Mol Hum Reprod. 2016;22:819–832.Google Scholar
Liu, F, Cai, C, Wu, X, et al. Effect of KnockOut serum replacement on germ cell development of immature testis tissue culture. Theriogenology. 2016;85:193–199.Google Scholar
Perrard, MH, Sereni, N, Schluth-Bolard, C, et al. Complete human and rat ex vivo spermatogenesis from fresh or frozen testicular tissue. Biol Reprod. 2016;95:89.Google Scholar
Komeya, M, Kimura, H, Nakamura, H, et al. Long-term ex vivo maintenance of testis tissues producing fertile sperm in a microfluidic device. Sci Rep. 2016;6:21472.Google Scholar
Komeya, M, Hayashi, K, Nakamura, H, et al. Pumpless microfluidic system driven by hydrostatic pressure induces and maintains mouse spermatogenesis in vitro. Sci Rep. 2017;7(1):15459.Google Scholar
Reda, A, Albalushi, H, Montalvo, SC, et al. Knock-out serum replacement and melatonin effects on germ cell differentiation in murine testicular explant cultures. Ann Biomed Eng. 2017;45:1783–1794.Google Scholar
Rondanino, C, Maouche, A, Dumont, L, Oblette, A, Rives, N. Establishment, maintenance and functional integrity of the blood-testis barrier in organotypic cultures of fresh and frozen/thawed prepubertal mouse testes. Mol Hum Reprod. 2017;23:304–320.Google Scholar
Stukenborg, J-B, Alves-Lopes, JP, Kurek, M, et al. Spermatogonial quantity in human prepubertal testicular tissue collected for fertility preservation prior to potentially sterilizing therapy. Hum Reprod. 2018;33(9):1677–1683.Google Scholar
Medrano, JV, Vilanova-Pérez, T, Fornés-Ferrer, V, et al. Influence of temperature, serum, and gonadotropin supplementation in short- and long-term organotypic culture of human immature testicular tissue. Fertil Steril. 2018;110(6):1045–1057.Google Scholar
Yamanaka, H, Komeya, M, Nakamura, H, et al. A monolayer microfluidic device supporting mouse spermatogenesis with improved visibility. Biochem BioPhys Res Commun. 2018;500(4):885–891.Google Scholar
Portela, JMD, de Winter-Korver, CM, van Daalen, SKM, et al. Assessment of fresh and cryopreserved testicular tissues from (pre)pubertal boys during organ culture as a strategy for in vitro spermatogenesis. Hum Reprod. 2019;34(12):2443–2455.Google Scholar
Ghatnekar, R, Lima‐De‐faria, A, Rubin, S, Menander, K. Development of human male meiosis in vitro. Hereditas. 1974;78:265–271.Google Scholar
Eddy, EM, Kahri, AI. Cell associations and surface features in cultures of juvenile rat seminiferous tubules. Anat Rec. 1976;185:333–357.Google Scholar
Aizawa, S, Nishimune, Y. In‐vitro differentiation of type A spermatogonia in mouse cryptorchid testis. J Reprod Fertil. 1979;56:99–104.Google Scholar
Curtis, D. In vitro differentiation of diakinesis figures in human testis. Hum Genet. 1981;59:406–411.Google Scholar
Nishimune, YM, Osaka, M. In vitro differentiation mouse cryptorchid of type a spermatogonia from testes in serum‐free. Biol Reprod. 1983;28:1217–1223.Google Scholar
Parvinen, M, Wright, WW, Phillips, DM, Mather, NA, Musto, NA, Bardin, CW. Spermatogenesis in vitro: completion of meiosis and early spermiogenesis. Endocrinology. 1983;112:1150–1152.Google Scholar
Toppari, J, Mali, P, Eerola, E. Rat spermatogenesis in vitro traced by quantitative flow cytometry. J Histochem Cytochem. 1986;34:1029–1035.Google Scholar
Kim, KJ, Kim, BG, Kim, YH, et al. In vitro spermatogenesis using bovine testis tissue culture techniques. Tissue Eng Regener Med. 2015;12:314–323.Google Scholar
Arkoun, B, Dumont, L, Milazzo, JP, et al. Retinol improves in vitro differentiation of pre-pubertal mouse spermatogonial stem cells into sperm during the first wave of spermatogenesis. PLoS ONE. 2015;10:e0116660.Google Scholar
Dumont, L, Arkoun, B, Jumeau, F, Milazzo, J-F, Bironneau, A, Liot, D, Wils, J, Rondanino, C, Rives, N. Assessment of the optimal vitrification protocol for pre-pubertal mice testes leading to successful in vitro production of flagellated spermatozoa. Andrology. 2015; 3(3):611–625.Google Scholar
Sato, T, Katagiri, K, Kojima, K, Komeya, M, Yao, M, Ogawa, T. In vitro spermatogenesis in explanted adult mouse testis tissues. PLoS ONE. 2015;10:e0130171.Google Scholar
de Michele, F, Poels, J, Weerens, L, et al. Preserved seminiferous tubule integrity with spermatogonial survival and induction of Sertoli and Leydig cell maturation after long-term organotypic culture of prepubertal human testicular tissue. Hum Reprod. 2017a;32:32–45.Google Scholar
de Michele, F, Vermeulen, M, Wyns, C. Fertility restoration with spermatogonial stem cells. Curr Opin Endocrinol Diabetes Obes. 2017b;24:424–431.Google Scholar
Gholami, K, Vermeulen, M, Del Vento, F, de Michele, F, Giudice, MG, Wyns, C. The air-liquid interface culture of the mechanically isolated seminiferous tubules embedded in agarose or alginate improves in vitro spermatogenesis at the expense of attenuating their integrity. In Vitro Cell Dev Biol Anim. 2020;56(3):261–270.Google Scholar
Yokonishi, T, Sato, T, Komeya, M, et al. Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun. 2014;5:4320.Google Scholar
Steinberger, A, Steinberger, E. In vitro culture of rat testicular cells. Exptl Cell Res. 1966;44:443–452.Google Scholar
Rassoulzadegan, M, Paquis-Flucklinger, V, Bertino, B, et al. Transmeiotic differentiation of male germ cells in culture. Cell. 1993; 75(5):997–1006.Google Scholar
Marh, J, Tres, LL, Yamazaki, Y, Yanagimachi, R, Kierszenbaum, AL. Mouse round spermatids developed in vitro from preexisting spermatocytes can produce normal offspring by nuclear injection into in vivo‐developed mature oocytes. Biol Reprod. 2003;69:169–176.Google Scholar
Hofmann, MC, Hess, RA, Goldberg, E, Millán, JL. Immortalized germ cells undergo meiosis in vitro. PNAS, 1994; 91(12): 5533–5537.Google Scholar
Hasegawa, H, Terada, Y, Ugajin, T, Yaegashi, N, Sato, K. A novel culture system for mouse spermatid maturation which produces elongating spermatids capable of inducing calcium oscillation during fertilization and embryonic development. J Assist Reprod Genet. 2010;27(9–10):565–570.Google Scholar
Izadyar, F, Den Ouden, K, Creemers, LB, Posthuma, G, Parvinen, M, De Rooij, DG. Proliferation and differentiation of bovine type A spermatogonia during long-term culture. Biol Reprod. 2003;68(1):272–281.Google Scholar
Grinspon, RP, Rey, RA. Molecular characterization of XX maleness. Int J Mol Sci. 2019;20:6089.Google Scholar
Steinberger, A, Steinberger, E, Perloff, WH. Growth of rat testes fragments in organ culture. Fed Proc. 1963;22:372.Google Scholar
Steinberger, A, Steinberger, E. Stimulatory effect of vitamins and glutamine on the differentiation of germ cells in rat testes organ culture grown in chemically defined media. Exp Cell Res. 1966;44:429–435.Google Scholar
Parvinen, M, Vanha-Perttula, T. Identification and enzyme quantification of the stages of the seminiferous epithelial wave in the rat. Anat Rec. 1972;174:435–449.Google Scholar
Alves-Lopes, JP, Söder, O, Stukenborg, JB. Use of a three-layer gradient system of cells for rat testicular organoid generation. Nat Protoc. 2018;13:248–259.Google Scholar

References

Agarwal, A, Mulgund, A, Hamada, A, Chyatte, MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 2015;13:37.Google Scholar
Esteves, SC. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl. 2015;17(3):459–470.Google Scholar
Foresta, C, Garolla, A, Bartoloni, L, Bettella, A, Ferlin, A. Genetic abnormalities among severely oligospermic men who are candidates for intracytoplasmic sperm injection. J Clin Endocrinol Metab. 2005;90(1):152–156.Google Scholar
Georgiou, I, Syrrou, M, Pardalidis, N, et al. Genetic and epigenetic risks of intracytoplasmic sperm injection method. Asian J Androl. 2006;8(6):643–673.Google Scholar
O’Flynn O’Brien, KL, Varghese, AC, Agarwal, A. The genetic causes of male factor infertility: a review. Fertil Steril. 2010;93(1):1–12.Google Scholar
Gassei, K, Orwig, KE. Experimental methods to preserve male fertility and treat male infertility. Fertil Steril. 2016;105(2):256–266.Google Scholar
Lim, J, Goriely, A, Turner, GD, et al. OCT2, SSX and SAGE1 reveal the phenotypic heterogeneity of spermatocytic seminoma reflecting distinct subpopulations of spermatogonia. J Pathol. 2011;224(4):473–483.Google Scholar
Looijenga, LHJ, Hersmus, R, Gillis, AJM, et al. Genomic and expression profiling of human spermatocytic seminomas: primary spermatocyte as tumorigenic precursor and DMRT1 as candidate chromosome 9 gene. Cancer Res. 2006;66(1):290–302.Google Scholar
Clermont, Y. Renewal of spermatogonia in man. Am J Anat. 1966;118(2):509–524.Google Scholar
Clermont, Y. Spermatogenesis in man: a study of the spermatogonial population. Fertil Steril. 1966;17(6):705–721.Google Scholar
Clermont, Y. Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops). Am J Anat. 1969;126(1):57–71.Google Scholar
Grisanti, L, Falciatori, I, Grasso, M, et al. Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells. 2009;27(12):3043–3052.Google Scholar
Altman, E, Yango, P, Moustafa, R, Smith, JF, Klatsky, PC, Tran, ND. Characterization of human spermatogonial stem cell markers in fetal, pediatric, and adult testicular tissues. Reproduction. 2014;148(4):417–427.Google Scholar
Kubota, H, Avarbock, MR, Brinster, RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 2004;101(47):16489–16494.Google Scholar
Brinster, RL, Avarbock, MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11303–11307.Google Scholar
Brinster, RL, Zimmermann, JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11298–11302.Google Scholar
Guo, J, Grow, EJ, Mlcochova, H, et al. The adult human testis transcriptional cell atlas. Cell Res. 2018;28(12):1141.Google Scholar
Yoshida, S, Sukeno, M, Nakagawa, T, et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development. 2006;133(8):1495–1505.Google Scholar
Tegelenbosch, RA, de Rooij, DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 1993;290(2):193–200.Google Scholar
Hara, K, Nakagawa, T, Enomoto, H, et al. Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell. 2014;14(5):658–672.Google Scholar
Helsel, AR, Yang, Q-E, Oatley, MJ, Lord, T, Sablitzky, F, Oatley, JM. ID4 levels dictate the stem cell state in mouse spermatogonia. Dev Camb Engl. 2017;144(4):624–634.Google Scholar
Honaramooz, A, Snedaker, A, Boiani, M, Schöler, H, Dobrinski, I, Schlatt, S. Sperm from neonatal mammalian testes grafted in mice. Nature. 2002;418(6899):778–781.Google Scholar
Liu, Z, Nie, Y-H, Zhang, C-C, et al. Generation of macaques with sperm derived from juvenile monkey testicular xenografts. Cell Res. 2016;26(1):139–142.Google Scholar
Wistuba, J, Mundry, M, Luetjens, CM, Schlatt, S. Cografting of hamster (Phodopus sungorus) and marmoset (Callithrix jacchus) testicular tissues into nude mice does not overcome blockade of early spermatogenic differentiation in primate grafts. Biol Reprod. 2004;71(6):2087–2091.Google Scholar
Goossens, E, Geens, M, De Block, G, Tournaye, H. Spermatogonial survival in long-term human prepubertal xenografts. Fertil Steril. 2008;90(5):2019–2022.Google Scholar
Fayomi, AP, Peters, K, Sukhwani, M, et al. Autologous grafting of cryopreserved prepubertal rhesus testis produces sperm and offspring. Science. 2019;363(6433):1314–1319.Google Scholar
Dovey, SL, Valli, H, Hermann, BP, et al. Eliminating malignant contamination from therapeutic human spermatogonial stem cells. J Clin Invest. 2013;123(4):1833–1843.Google Scholar
Hou, M, Andersson, M, Zheng, C, Sundblad, A, Söder, O, Jahnukainen, K. Immunomagnetic separation of normal rat testicular cells from Roser’s T-cell leukaemia cells is ineffective. Int J Androl. 2009;32(1):66–73.Google Scholar
Kanatsu-Shinohara, M, Ogonuki, N, Inoue, K, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69(2):612–616.Google Scholar
Sadri-Ardekani, H, Mizrak, SC, van Daalen, SKM, et al. Propagation of human spermatogonial stem cells in vitro. JAMA. 2009;302(19):2127–2134.Google Scholar
Sadri-Ardekani, H, Akhondi, MA, van der Veen, F, Repping, S, van Pelt, AMM. In vitro propagation of human prepubertal spermatogonial stem cells. JAMA. 2011;305(23):2416–2418.Google Scholar
Dong, L, Kristensen, SG, Hildorf, S, et al. Propagation of spermatogonial stem cell-like cells from infant boys. Front Physiol. 2019;10:1155.Google Scholar
Sato, T, Katagiri, K, Gohbara, A, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471(7339):504–507.Google Scholar
Medrano, JV, Vilanova-Pérez, T, Fornés-Ferrer, V, et al. Influence of temperature, serum, and gonadotropin supplementation in short- and long-term organotypic culture of human immature testicular tissue. Fertil Steril. 2018;110(6):1045–1057.e3.Google Scholar
de Michele, F, Poels, J, Vermeulen, M, et al. Haploid germ cells generated in organotypic culture of testicular tissue from prepubertal boys. Front Physiol. 2018;9:1413.Google Scholar
Alves-Lopes, JP, Söder, O, Stukenborg, J-B. Testicular organoid generation by a novel in vitro three-layer gradient system. Biomaterials. 2017;130:76–89.Google Scholar
Mulder, CL, Zheng, Y, Jan, SZ, et al. Spermatogonial stem cell autotransplantation and germline genomic editing: a future cure for spermatogenic failure and prevention of transmission of genomic diseases. Hum Reprod Update. 2016;22(5):561–573.Google Scholar
Shimizu, T, Shiohara, M, Tai, T, Nagao, K, Nakajima, K, Kobayashi, H. Derivation of integration‐free iPSCs from a Klinefelter syndrome patient. Reprod Med Biol. 2015;15(1):35–43.Google Scholar
Zhao, Y, Ye, S, Liang, D, et al. In vitro modeling of human germ cell development using pluripotent stem cells. Stem Cell Rep. 2018;10(2):509–523.Google Scholar
Fujimoto, T, Miyayama, Y, Fuyuta, M. The origin, migration and fine morphology of human primordial germ cells. Anat Rec. 1977;188(3):315–330.Google Scholar
Hiller, M, Liu, C, Blumenthal, PD, Gearhart, JD, Kerr, CL. Bone morphogenetic protein 4 mediates human embryonic germ cell derivation. Stem Cells Dev. 2011;20(2):351–361.Google Scholar
Sasaki, K, Yokobayashi, S, Nakamura, T, et al. Robust in vitro induction of human germ cell fate from pluripotent stem cells. Cell Stem Cell. 2015;17(2):178–194.Google Scholar
Clark, AT, Bodnar, MS, Fox, M, et al. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet. 2004;13(7):727–739.Google Scholar
Fox, N, Damjanov, I, Martinez-Hernandez, A, Knowles, BB, Solter, D. Immunohistochemical localization of the early embryonic antigen (SSEA-1) in postimplantation mouse embryos and fetal and adult tissues. Dev Biol. 1981;83(2):391–398.Google Scholar
Mouka, A, Tachdjian, G, Dupont, J, Drévillon, L, Tosca, L. In vitro gamete differentiation from pluripotent stem cells as a promising therapy for infertility. Stem Cells Dev. 2016;25(7):509–521.Google Scholar
Koopman, P, Münsterberg, A, Capel, B, Vivian, N, Lovell-Badge, R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature. 1990;348(6300):450–452.Google Scholar
Geens, M, Sermon, KD, Van de Velde, H, Tournaye, H. Sertoli cell-conditioned medium induces germ cell differentiation in human embryonic stem cells. J Assist Reprod Genet. 2011;28(5):471–480.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×